Review ArticleRecent Developments for Remediating Acidic Mine WatersUsing Sulfidogenic Bacteria
Ivan Nancucheo1 Joseacute A P Bitencourt2 Prafulla K Sahoo2 Joner Oliveira Alves3
Joseacute O Siqueira2 and Guilherme Oliveira2
1Facultad de Ingenierıa y Tecnologıa Universidad San Sebastian Lientur 1457 4080871 Concepcion Chile2Instituto Tecnologico Vale Rua Boaventura da Silva 955 66055-090 Belem PA Brazil3SENAI Innovation Institute for Mineral Technologies Av Com Bras de Aguiar 548 66035-405 Belem PA Brazil
Correspondence should be addressed to Ivan Nancucheo inancucheogmailcomand Guilherme Oliveira guilhermeoliveiraitvorg
Received 27 March 2017 Revised 31 July 2017 Accepted 23 August 2017 Published 3 October 2017
Academic Editor Raluca M Hlihor
Copyright copy 2017 Ivan Nancucheo et alThis is an open access article distributed under theCreativeCommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited
Acidic mine drainage (AMD) is regarded as a pollutant and considered as potential source of valuable metals With diminishingmetal resources and ever-increasing demand on industry recovering AMD metals is a sustainable initiative despite facing majorchallenges AMD refers to effluents draining from abandoned mines and mine wastes usually highly acidic that contain a varietyof dissolved metals (Fe Mn Cu Ni and Zn) in much greater concentration than what is found in natural water bodies Thereare numerous remediation treatments including chemical (lime treatment) or biological methods (aerobic wetlands and compostbioreactors) used for metal precipitation and removal from AMD However controlled biomineralization and selective recoveringof metals using sulfidogenic bacteria are advantageous reducing costs and environmental risks of sludge disposal The increasedunderstanding of the microbiology of acid-tolerant sulfidogenic bacteria will lead to the development of novel approaches to AMDtreatment We present and discuss several important recent approaches using low sulfidogenic bioreactors to both remediateand selectively recover metal sulfides from AMD This work also highlights the efficiency and drawbacks of these types oftreatments formetal recovery and points to future research for enhancing the use of novel acidophilic and acid-tolerant sulfidogenicmicroorganisms in AMD treatment
1 Introduction
Metal mining provides everyday goods and services essentialto society However this activity has at times caused extensiveand sometimes severe pollution of air vegetation and waterbodies [1] Streams draining active or abandoned mines andmine spoils are widely considered as hazardous to humanhealth and the environment but on the other hand they mayalso be alternative potential sources of valuable metals [2 3]
Currently millions of tons of ores are processed everyyear by the mining industry and are disposed in the formof waste rocks and mine tailings As higher-grade ores arediminishing the primary ores that are processed by miningcompanies are of increasingly lower grade (metal content)and the growing amount of waste material produced bymining operations is consequently significant The use oflower grade ore was made possible by the development of the
flotation technique in the late 19th century which allowed theseparation of metal sulfide minerals from gangue mineralsthat have no commercial value [4] As a result of selectiveflotation about 95 to 99 of the ground primary ores endup as fine-grain tailings in the case of copper ores Thecomposition of tailings is directly dependent on that of theore and therefore they are highly variable though pyrite(FeS2) is frequently the most reactive and dominant sulfide
mineral present in tailings wastes [4ndash6]Pyritic mine tailings therefore have the potential to
become extremely acidic when in contact with surface waterUnder oxidizing conditions pyrite-bearing wastes producesulfuric acid The acidic water further dissolves other metalscontained in mine waste resulting in low pH water enrichedwith soluble sulfate Fe Al and other transition metalsknown as acid mine drainage (AMD) (Figure 1) [7 8]
HindawiBioMed Research InternationalVolume 2017 Article ID 7256582 17 pageshttpsdoiorg10115520177256582
2 BioMed Research International
(a) (b)
(c) (d)
(e) (f)
Figure 1 Illustration of streams of acidicwaters draining fromactive or abandonedmines andmine spoils (a)AMD froma coppermine in theState of Para Brazil that has been remediated with limestone treatment (b) acidic water released from abandoned undergroundmetalliferousmine in the Republic of South Africa (reproduced fromAkcil and Koldas [9]) (c) acidic mine water draining from an abandoned sulfurminenorthern Chile (d) AMD discharge in the Lomero-Poyatos mine Spain (reproduced from Espana et al [10]) (e) acidic water draining fromCoal mines Jaintia Hills and (f) AMD originated from mine tailings Canada (reproduced from Burtnyski [11])
BioMed Research International 3
2 Remediation of Acidic Mine Water
Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]
A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD
There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo
systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world
The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]
TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]
The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H
2S to recover up to
12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]
Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow
4 BioMed Research International
Table1Summaryof
thevario
ustypeso
ftreatmentfor
AMD
(com
piledfro
mSaho
oet
al[15]Gazea
etal[36]Trum
m[37]T
aylore
tal[38]R
oyCh
owdh
uryet
al[39]John
sonand
Hallberg[22]Skousen
[40]Skousen
etal[41]andSeervietal[42])
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nBiologica
l
Aerobicw
etland
(AeW
)Mod
eratea
ciditynetalkalin
emined
rainage
Organicmattersoillim
estone
gravel
Oxidatio
nhydrolysis
precipitatio
nRe
quire
dlonger
detentiontim
eandhu
gesurfa
cearea
Anaerob
icwetland
(AnW
)Net-acidicw
ater
with
high
AlFe
andDO
Organicmattersuch
ascompo
stsawdu
sthayandlim
estone
gravel
Sulfateredu
ction
metal
precipitateas
sulfidesmicrobial
generatedalkalin
ityRe
quire
dlong
resid
ence
time
Verticalflo
wwetland
(VFW
)Net-acidicw
ater
with
high
AlFe
andDO
Limestoneorganicmatter
SulfateandFe
redu
ction
acid
neutralization
Highcapitalcostpo
tentialfor
armoringandplug
ging
with
hydroxides
Sulfateredu
cing
bioreactor
(SRB
)Sm
allfl
owso
rtosituatio
nsvery
acidicandmetalric
hwater
Organicsubstrates
uchas
hay
alfalfasaw
dust
paper
woo
dchipscrushed
limestone
andcompo
stor
manure
Microbialsulfateredu
ction
Highcapitalcostextre
mely
low
pHseverelyim
pactthee
fficiency
ofSredu
cing
bacteria
Pyrolusitelim
estone
beds
Mod
eratep
Handwhere
majority
ofacidity
isrelated
toMn
Limestoneorganicsubstrate
aerobicm
icroorganism
Hydrolysis
ofMn
Not
suitablefor
drainage
which
contains
high
Fehigh
maintenance
Perm
eabler
eactiveb
arrie
rs(PRB
)Groun
dwaterlow
DO
Organicmatterlim
estonezero
valent
iron
Sulfateredu
ction
sulfide
precipitates
neutralization
Iron
-oxidizing
bioreactor
Acidicwater
Fe-oxidizing
bacteriaand
archaea
Feoxidation
Phytorem
ediatio
nAny
AMD-im
pacted
sites
Metaltolerant
plantspecies
Phytoextractionand
phytostabilization
Successd
epends
onthep
roper
selectionof
the
metal-hyperaccumulator
plant
BioMed Research International 5
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nGeochem
ical
Ano
xiclim
estone
drain(A
LD)
Acidicwater
with
lowAlFeD
OLimestone
gravel
compacted
soil
Limestone
dissolution
raise
pH
precipitatio
n
Fe-oxide
armoringlim
estone
limitperm
eabilityandcause
plug
ging
Alkalinity
prod
ucingsyste
m(A
PS)
Acidicwater
Organicmatterlim
estone
Ano
xicc
onditio
nneutralization
precipitatio
n
Openlim
estone
channel(OLC
)Re
quire
dste
epslo
pesnet-a
cidic
water
with
high
AlFe
andDO
Limestone
Limestone
dissolution
neutralization
Arm
oringor
thec
oatin
gof
the
limestonelarge
amou
ntis
neededdecreases
the
neutralizingcapacity
Limestone
leachbed(LLB
)Lo
wpH
andmetal-fr
eewater
Limestone
Limestone
dissolution
neutralization
Arm
oringwith
Fehydroxides
Steel-slagleachbed(SLB
)Highlyacidicandmetal-fr
eewater
Steelslag
Raise
alkalin
ityneutralization
Not
suitablefor
metal-la
den
water
Limestone
diversionwe
lls(LDW)
Sitesthato
ffera
suitable
topo
graphicalfall
Crushedlim
estone
aggregate
Hydraulicforcehydrolysis
and
neutralization
Requ
iredrefillin
gwith
limestone
every2ndash4weeks
Limestone
sand
Stream
flowwater
Sand
-sized
limestone
neutralizingacid
Coatin
gof
limestone
Low-pHFe
oxidationchannels
Shallowchannels
Limestone
orsand
stone
aggregate
Feoxidation
adsorptio
nand
coprecipitatio
n
Itremoves
someF
ebu
trem
oval
efficiency
hasn
otbeen
determ
ined
Sulfide
passivationmicroencapsulation
Pitw
allfacessulfid
ebearin
gwastesrocks
piles
Inorganicc
oatin
gph
osph
ate
silicafly
ashlim
estoneorganic
coatinghu
micacidlipids
polyethylene
polyam
ine
alkoxysilanesfattyacidoxalic
acidcatecho
l
Preventsulfid
eoxidatio
nby
inorganica
ndorganicc
oatin
g
Long
-term
effectiv
enessisstillin
questio
norganicc
oatin
gexpensive
Electro
chem
icalcover
Tailing
wasterock
Con
ductives
teelmeshcathod
emetalanod
eRe
ducing
DOby
electrochem
ical
process
Highcapitalcosto
fano
desno
inform
ationavailableo
nlarge
scalea
pplication
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
2 BioMed Research International
(a) (b)
(c) (d)
(e) (f)
Figure 1 Illustration of streams of acidicwaters draining fromactive or abandonedmines andmine spoils (a)AMD froma coppermine in theState of Para Brazil that has been remediated with limestone treatment (b) acidic water released from abandoned undergroundmetalliferousmine in the Republic of South Africa (reproduced fromAkcil and Koldas [9]) (c) acidic mine water draining from an abandoned sulfurminenorthern Chile (d) AMD discharge in the Lomero-Poyatos mine Spain (reproduced from Espana et al [10]) (e) acidic water draining fromCoal mines Jaintia Hills and (f) AMD originated from mine tailings Canada (reproduced from Burtnyski [11])
BioMed Research International 3
2 Remediation of Acidic Mine Water
Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]
A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD
There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo
systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world
The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]
TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]
The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H
2S to recover up to
12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]
Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow
4 BioMed Research International
Table1Summaryof
thevario
ustypeso
ftreatmentfor
AMD
(com
piledfro
mSaho
oet
al[15]Gazea
etal[36]Trum
m[37]T
aylore
tal[38]R
oyCh
owdh
uryet
al[39]John
sonand
Hallberg[22]Skousen
[40]Skousen
etal[41]andSeervietal[42])
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nBiologica
l
Aerobicw
etland
(AeW
)Mod
eratea
ciditynetalkalin
emined
rainage
Organicmattersoillim
estone
gravel
Oxidatio
nhydrolysis
precipitatio
nRe
quire
dlonger
detentiontim
eandhu
gesurfa
cearea
Anaerob
icwetland
(AnW
)Net-acidicw
ater
with
high
AlFe
andDO
Organicmattersuch
ascompo
stsawdu
sthayandlim
estone
gravel
Sulfateredu
ction
metal
precipitateas
sulfidesmicrobial
generatedalkalin
ityRe
quire
dlong
resid
ence
time
Verticalflo
wwetland
(VFW
)Net-acidicw
ater
with
high
AlFe
andDO
Limestoneorganicmatter
SulfateandFe
redu
ction
acid
neutralization
Highcapitalcostpo
tentialfor
armoringandplug
ging
with
hydroxides
Sulfateredu
cing
bioreactor
(SRB
)Sm
allfl
owso
rtosituatio
nsvery
acidicandmetalric
hwater
Organicsubstrates
uchas
hay
alfalfasaw
dust
paper
woo
dchipscrushed
limestone
andcompo
stor
manure
Microbialsulfateredu
ction
Highcapitalcostextre
mely
low
pHseverelyim
pactthee
fficiency
ofSredu
cing
bacteria
Pyrolusitelim
estone
beds
Mod
eratep
Handwhere
majority
ofacidity
isrelated
toMn
Limestoneorganicsubstrate
aerobicm
icroorganism
Hydrolysis
ofMn
Not
suitablefor
drainage
which
contains
high
Fehigh
maintenance
Perm
eabler
eactiveb
arrie
rs(PRB
)Groun
dwaterlow
DO
Organicmatterlim
estonezero
valent
iron
Sulfateredu
ction
sulfide
precipitates
neutralization
Iron
-oxidizing
bioreactor
Acidicwater
Fe-oxidizing
bacteriaand
archaea
Feoxidation
Phytorem
ediatio
nAny
AMD-im
pacted
sites
Metaltolerant
plantspecies
Phytoextractionand
phytostabilization
Successd
epends
onthep
roper
selectionof
the
metal-hyperaccumulator
plant
BioMed Research International 5
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nGeochem
ical
Ano
xiclim
estone
drain(A
LD)
Acidicwater
with
lowAlFeD
OLimestone
gravel
compacted
soil
Limestone
dissolution
raise
pH
precipitatio
n
Fe-oxide
armoringlim
estone
limitperm
eabilityandcause
plug
ging
Alkalinity
prod
ucingsyste
m(A
PS)
Acidicwater
Organicmatterlim
estone
Ano
xicc
onditio
nneutralization
precipitatio
n
Openlim
estone
channel(OLC
)Re
quire
dste
epslo
pesnet-a
cidic
water
with
high
AlFe
andDO
Limestone
Limestone
dissolution
neutralization
Arm
oringor
thec
oatin
gof
the
limestonelarge
amou
ntis
neededdecreases
the
neutralizingcapacity
Limestone
leachbed(LLB
)Lo
wpH
andmetal-fr
eewater
Limestone
Limestone
dissolution
neutralization
Arm
oringwith
Fehydroxides
Steel-slagleachbed(SLB
)Highlyacidicandmetal-fr
eewater
Steelslag
Raise
alkalin
ityneutralization
Not
suitablefor
metal-la
den
water
Limestone
diversionwe
lls(LDW)
Sitesthato
ffera
suitable
topo
graphicalfall
Crushedlim
estone
aggregate
Hydraulicforcehydrolysis
and
neutralization
Requ
iredrefillin
gwith
limestone
every2ndash4weeks
Limestone
sand
Stream
flowwater
Sand
-sized
limestone
neutralizingacid
Coatin
gof
limestone
Low-pHFe
oxidationchannels
Shallowchannels
Limestone
orsand
stone
aggregate
Feoxidation
adsorptio
nand
coprecipitatio
n
Itremoves
someF
ebu
trem
oval
efficiency
hasn
otbeen
determ
ined
Sulfide
passivationmicroencapsulation
Pitw
allfacessulfid
ebearin
gwastesrocks
piles
Inorganicc
oatin
gph
osph
ate
silicafly
ashlim
estoneorganic
coatinghu
micacidlipids
polyethylene
polyam
ine
alkoxysilanesfattyacidoxalic
acidcatecho
l
Preventsulfid
eoxidatio
nby
inorganica
ndorganicc
oatin
g
Long
-term
effectiv
enessisstillin
questio
norganicc
oatin
gexpensive
Electro
chem
icalcover
Tailing
wasterock
Con
ductives
teelmeshcathod
emetalanod
eRe
ducing
DOby
electrochem
ical
process
Highcapitalcosto
fano
desno
inform
ationavailableo
nlarge
scalea
pplication
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 3
2 Remediation of Acidic Mine Water
Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]
A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD
There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo
systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world
The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]
TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]
The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H
2S to recover up to
12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]
Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow
4 BioMed Research International
Table1Summaryof
thevario
ustypeso
ftreatmentfor
AMD
(com
piledfro
mSaho
oet
al[15]Gazea
etal[36]Trum
m[37]T
aylore
tal[38]R
oyCh
owdh
uryet
al[39]John
sonand
Hallberg[22]Skousen
[40]Skousen
etal[41]andSeervietal[42])
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nBiologica
l
Aerobicw
etland
(AeW
)Mod
eratea
ciditynetalkalin
emined
rainage
Organicmattersoillim
estone
gravel
Oxidatio
nhydrolysis
precipitatio
nRe
quire
dlonger
detentiontim
eandhu
gesurfa
cearea
Anaerob
icwetland
(AnW
)Net-acidicw
ater
with
high
AlFe
andDO
Organicmattersuch
ascompo
stsawdu
sthayandlim
estone
gravel
Sulfateredu
ction
metal
precipitateas
sulfidesmicrobial
generatedalkalin
ityRe
quire
dlong
resid
ence
time
Verticalflo
wwetland
(VFW
)Net-acidicw
ater
with
high
AlFe
andDO
Limestoneorganicmatter
SulfateandFe
redu
ction
acid
neutralization
Highcapitalcostpo
tentialfor
armoringandplug
ging
with
hydroxides
Sulfateredu
cing
bioreactor
(SRB
)Sm
allfl
owso
rtosituatio
nsvery
acidicandmetalric
hwater
Organicsubstrates
uchas
hay
alfalfasaw
dust
paper
woo
dchipscrushed
limestone
andcompo
stor
manure
Microbialsulfateredu
ction
Highcapitalcostextre
mely
low
pHseverelyim
pactthee
fficiency
ofSredu
cing
bacteria
Pyrolusitelim
estone
beds
Mod
eratep
Handwhere
majority
ofacidity
isrelated
toMn
Limestoneorganicsubstrate
aerobicm
icroorganism
Hydrolysis
ofMn
Not
suitablefor
drainage
which
contains
high
Fehigh
maintenance
Perm
eabler
eactiveb
arrie
rs(PRB
)Groun
dwaterlow
DO
Organicmatterlim
estonezero
valent
iron
Sulfateredu
ction
sulfide
precipitates
neutralization
Iron
-oxidizing
bioreactor
Acidicwater
Fe-oxidizing
bacteriaand
archaea
Feoxidation
Phytorem
ediatio
nAny
AMD-im
pacted
sites
Metaltolerant
plantspecies
Phytoextractionand
phytostabilization
Successd
epends
onthep
roper
selectionof
the
metal-hyperaccumulator
plant
BioMed Research International 5
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nGeochem
ical
Ano
xiclim
estone
drain(A
LD)
Acidicwater
with
lowAlFeD
OLimestone
gravel
compacted
soil
Limestone
dissolution
raise
pH
precipitatio
n
Fe-oxide
armoringlim
estone
limitperm
eabilityandcause
plug
ging
Alkalinity
prod
ucingsyste
m(A
PS)
Acidicwater
Organicmatterlim
estone
Ano
xicc
onditio
nneutralization
precipitatio
n
Openlim
estone
channel(OLC
)Re
quire
dste
epslo
pesnet-a
cidic
water
with
high
AlFe
andDO
Limestone
Limestone
dissolution
neutralization
Arm
oringor
thec
oatin
gof
the
limestonelarge
amou
ntis
neededdecreases
the
neutralizingcapacity
Limestone
leachbed(LLB
)Lo
wpH
andmetal-fr
eewater
Limestone
Limestone
dissolution
neutralization
Arm
oringwith
Fehydroxides
Steel-slagleachbed(SLB
)Highlyacidicandmetal-fr
eewater
Steelslag
Raise
alkalin
ityneutralization
Not
suitablefor
metal-la
den
water
Limestone
diversionwe
lls(LDW)
Sitesthato
ffera
suitable
topo
graphicalfall
Crushedlim
estone
aggregate
Hydraulicforcehydrolysis
and
neutralization
Requ
iredrefillin
gwith
limestone
every2ndash4weeks
Limestone
sand
Stream
flowwater
Sand
-sized
limestone
neutralizingacid
Coatin
gof
limestone
Low-pHFe
oxidationchannels
Shallowchannels
Limestone
orsand
stone
aggregate
Feoxidation
adsorptio
nand
coprecipitatio
n
Itremoves
someF
ebu
trem
oval
efficiency
hasn
otbeen
determ
ined
Sulfide
passivationmicroencapsulation
Pitw
allfacessulfid
ebearin
gwastesrocks
piles
Inorganicc
oatin
gph
osph
ate
silicafly
ashlim
estoneorganic
coatinghu
micacidlipids
polyethylene
polyam
ine
alkoxysilanesfattyacidoxalic
acidcatecho
l
Preventsulfid
eoxidatio
nby
inorganica
ndorganicc
oatin
g
Long
-term
effectiv
enessisstillin
questio
norganicc
oatin
gexpensive
Electro
chem
icalcover
Tailing
wasterock
Con
ductives
teelmeshcathod
emetalanod
eRe
ducing
DOby
electrochem
ical
process
Highcapitalcosto
fano
desno
inform
ationavailableo
nlarge
scalea
pplication
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
4 BioMed Research International
Table1Summaryof
thevario
ustypeso
ftreatmentfor
AMD
(com
piledfro
mSaho
oet
al[15]Gazea
etal[36]Trum
m[37]T
aylore
tal[38]R
oyCh
owdh
uryet
al[39]John
sonand
Hallberg[22]Skousen
[40]Skousen
etal[41]andSeervietal[42])
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nBiologica
l
Aerobicw
etland
(AeW
)Mod
eratea
ciditynetalkalin
emined
rainage
Organicmattersoillim
estone
gravel
Oxidatio
nhydrolysis
precipitatio
nRe
quire
dlonger
detentiontim
eandhu
gesurfa
cearea
Anaerob
icwetland
(AnW
)Net-acidicw
ater
with
high
AlFe
andDO
Organicmattersuch
ascompo
stsawdu
sthayandlim
estone
gravel
Sulfateredu
ction
metal
precipitateas
sulfidesmicrobial
generatedalkalin
ityRe
quire
dlong
resid
ence
time
Verticalflo
wwetland
(VFW
)Net-acidicw
ater
with
high
AlFe
andDO
Limestoneorganicmatter
SulfateandFe
redu
ction
acid
neutralization
Highcapitalcostpo
tentialfor
armoringandplug
ging
with
hydroxides
Sulfateredu
cing
bioreactor
(SRB
)Sm
allfl
owso
rtosituatio
nsvery
acidicandmetalric
hwater
Organicsubstrates
uchas
hay
alfalfasaw
dust
paper
woo
dchipscrushed
limestone
andcompo
stor
manure
Microbialsulfateredu
ction
Highcapitalcostextre
mely
low
pHseverelyim
pactthee
fficiency
ofSredu
cing
bacteria
Pyrolusitelim
estone
beds
Mod
eratep
Handwhere
majority
ofacidity
isrelated
toMn
Limestoneorganicsubstrate
aerobicm
icroorganism
Hydrolysis
ofMn
Not
suitablefor
drainage
which
contains
high
Fehigh
maintenance
Perm
eabler
eactiveb
arrie
rs(PRB
)Groun
dwaterlow
DO
Organicmatterlim
estonezero
valent
iron
Sulfateredu
ction
sulfide
precipitates
neutralization
Iron
-oxidizing
bioreactor
Acidicwater
Fe-oxidizing
bacteriaand
archaea
Feoxidation
Phytorem
ediatio
nAny
AMD-im
pacted
sites
Metaltolerant
plantspecies
Phytoextractionand
phytostabilization
Successd
epends
onthep
roper
selectionof
the
metal-hyperaccumulator
plant
BioMed Research International 5
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nGeochem
ical
Ano
xiclim
estone
drain(A
LD)
Acidicwater
with
lowAlFeD
OLimestone
gravel
compacted
soil
Limestone
dissolution
raise
pH
precipitatio
n
Fe-oxide
armoringlim
estone
limitperm
eabilityandcause
plug
ging
Alkalinity
prod
ucingsyste
m(A
PS)
Acidicwater
Organicmatterlim
estone
Ano
xicc
onditio
nneutralization
precipitatio
n
Openlim
estone
channel(OLC
)Re
quire
dste
epslo
pesnet-a
cidic
water
with
high
AlFe
andDO
Limestone
Limestone
dissolution
neutralization
Arm
oringor
thec
oatin
gof
the
limestonelarge
amou
ntis
neededdecreases
the
neutralizingcapacity
Limestone
leachbed(LLB
)Lo
wpH
andmetal-fr
eewater
Limestone
Limestone
dissolution
neutralization
Arm
oringwith
Fehydroxides
Steel-slagleachbed(SLB
)Highlyacidicandmetal-fr
eewater
Steelslag
Raise
alkalin
ityneutralization
Not
suitablefor
metal-la
den
water
Limestone
diversionwe
lls(LDW)
Sitesthato
ffera
suitable
topo
graphicalfall
Crushedlim
estone
aggregate
Hydraulicforcehydrolysis
and
neutralization
Requ
iredrefillin
gwith
limestone
every2ndash4weeks
Limestone
sand
Stream
flowwater
Sand
-sized
limestone
neutralizingacid
Coatin
gof
limestone
Low-pHFe
oxidationchannels
Shallowchannels
Limestone
orsand
stone
aggregate
Feoxidation
adsorptio
nand
coprecipitatio
n
Itremoves
someF
ebu
trem
oval
efficiency
hasn
otbeen
determ
ined
Sulfide
passivationmicroencapsulation
Pitw
allfacessulfid
ebearin
gwastesrocks
piles
Inorganicc
oatin
gph
osph
ate
silicafly
ashlim
estoneorganic
coatinghu
micacidlipids
polyethylene
polyam
ine
alkoxysilanesfattyacidoxalic
acidcatecho
l
Preventsulfid
eoxidatio
nby
inorganica
ndorganicc
oatin
g
Long
-term
effectiv
enessisstillin
questio
norganicc
oatin
gexpensive
Electro
chem
icalcover
Tailing
wasterock
Con
ductives
teelmeshcathod
emetalanod
eRe
ducing
DOby
electrochem
ical
process
Highcapitalcosto
fano
desno
inform
ationavailableo
nlarge
scalea
pplication
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 5
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nGeochem
ical
Ano
xiclim
estone
drain(A
LD)
Acidicwater
with
lowAlFeD
OLimestone
gravel
compacted
soil
Limestone
dissolution
raise
pH
precipitatio
n
Fe-oxide
armoringlim
estone
limitperm
eabilityandcause
plug
ging
Alkalinity
prod
ucingsyste
m(A
PS)
Acidicwater
Organicmatterlim
estone
Ano
xicc
onditio
nneutralization
precipitatio
n
Openlim
estone
channel(OLC
)Re
quire
dste
epslo
pesnet-a
cidic
water
with
high
AlFe
andDO
Limestone
Limestone
dissolution
neutralization
Arm
oringor
thec
oatin
gof
the
limestonelarge
amou
ntis
neededdecreases
the
neutralizingcapacity
Limestone
leachbed(LLB
)Lo
wpH
andmetal-fr
eewater
Limestone
Limestone
dissolution
neutralization
Arm
oringwith
Fehydroxides
Steel-slagleachbed(SLB
)Highlyacidicandmetal-fr
eewater
Steelslag
Raise
alkalin
ityneutralization
Not
suitablefor
metal-la
den
water
Limestone
diversionwe
lls(LDW)
Sitesthato
ffera
suitable
topo
graphicalfall
Crushedlim
estone
aggregate
Hydraulicforcehydrolysis
and
neutralization
Requ
iredrefillin
gwith
limestone
every2ndash4weeks
Limestone
sand
Stream
flowwater
Sand
-sized
limestone
neutralizingacid
Coatin
gof
limestone
Low-pHFe
oxidationchannels
Shallowchannels
Limestone
orsand
stone
aggregate
Feoxidation
adsorptio
nand
coprecipitatio
n
Itremoves
someF
ebu
trem
oval
efficiency
hasn
otbeen
determ
ined
Sulfide
passivationmicroencapsulation
Pitw
allfacessulfid
ebearin
gwastesrocks
piles
Inorganicc
oatin
gph
osph
ate
silicafly
ashlim
estoneorganic
coatinghu
micacidlipids
polyethylene
polyam
ine
alkoxysilanesfattyacidoxalic
acidcatecho
l
Preventsulfid
eoxidatio
nby
inorganica
ndorganicc
oatin
g
Long
-term
effectiv
enessisstillin
questio
norganicc
oatin
gexpensive
Electro
chem
icalcover
Tailing
wasterock
Con
ductives
teelmeshcathod
emetalanod
eRe
ducing
DOby
electrochem
ical
process
Highcapitalcosto
fano
desno
inform
ationavailableo
nlarge
scalea
pplication
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
6 BioMed Research International
Table1Con
tinued
Syste
mtype
Applicability
Supp
ortm
aterials
Mechanism
sLimitatio
nPh
ysica
l
Dry
cover
Sulfide
bearingwastesrockpiles
Fine-grained
soilorganic
materials
synthetic
material
(plasticliners)vegetation
Minim
izeo
xidatio
nby
physical
barrierneutralization
precipitates
Shortterm
effectiv
eness
Wetcover
Sulfide
wastes
Und
erwater
Disp
osingwasteun
derw
ater
anoxiccond
ition
sRe
quire
rigorou
seng
ineerin
gdesig
nhigh
maintenance
Gas
redo
xanddisplacement
syste
m(G
aRDS)
Und
ergrou
ndmines
CO2andCH4gas
Gas
mixturesp
hysic
allydisplace
O2
Itson
lyfeasiblewhere
partialor
completefl
ooding
isno
tfeasib
le
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 7
MetalSuldes(ZnS)
Air
Excess
Sulfur
Puriedeuent
Recycle
Neu
troph
ilic
SRB
Bior
eact
or o
ne
Bior
eact
or tw
oSu
lde
oxid
ising
bac
teriaWaste water or
process water(34
2minus and metalssuch as H
2+)
(2-rich gas
2
(3minus
(3I)
34
2minus+ 4(2 + (
+rarr (3
minus+ 4(2
H2+
+ (3minusrarr H3 + (
+
2(3minus+ 2 + 2(
+rarr 23
I+ 2(2
(a)
Bior
eact
orsta
ge I
Stag
e II
Ana
erob
ic ag
itate
dco
ntac
tor
SulfurReagents
Feed water(AMD)
sulfu
r red
ucin
g ba
cter
ia
ClarierTreated water
Filter
Metal sulde (ZnS)to smelter
(23
Gen
erat
ion
by
(23
(b)
Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])
simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate
stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
8 BioMed Research International
solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]
4C3H8O3+ 10H+ + 7SO
4
2minus+ Cu2+ + Zn2+ + Fe2+
997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H
2O
(1)
This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD
Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H
2S) by the SRB and orpiment
(As2S3) generated within the bioreactor In addition this
process was also observed to occur naturally in an acidic pitlake [31]
Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for
the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes
3 Microbiology in Remediating AcidicMine Waters
Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]
Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 9
Table2Isolated
sulfido
genicm
icroorganism
sand
theirm
aincharacteris
tics
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermocladium
modestiu
s45ndash82
(75)
26ndash
59(40)
Glycogen
starch
proteins
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
mud
)Japan
[43ndash45]
Caldivirg
amaquilin
gensis
70ndash9
023ndash64(37ndash4
2)
Glycogen
beefextract
pepton
etryptoneyeast
extract
Sulfu
rthiosulfate
L-cyste
ine
Hot
sprin
gs(w
ater
solfataric
soilmud
)Mt
Maquilin
gPh
ilipp
ines
[46]
Archaeoglobu
slithotro
phicu
snd
60
Acetate
SulfateL-cysteine
nd[4748]
Archaeoglobu
sveneficus
nd69
H2acetateformate
pyruvateyeastextract
citratelactatesta
rch
pepton
e
Sulfitethiosulfate
Wallsof
activ
eblack
smoker
atmiddle
AtlanticRidge
[44]
Archaeoglobu
sprofund
usnd
45ndash75
H2acetatepyruvate
yeastextractlactate
meatextractpeptone
crud
eoilwith
acetate
Sulfatethiosulfate
sulfite
Deepseah
ydrothermal
syste
moff
Guaym
as
Mexico
[4950]
Archaeoglobu
sfulgidu
s60ndash75
(70)
55ndash75
(60)
H2C
O2formate
form
amideD(minus)-and
L(+)-lactateglucose
starchcalam
inea
cids
pepton
egelatincasein
meatextractyeast
extract
Sulfatethiosulfate
sulfite
Marineh
ydrothermal
syste
mN
eron
eIta
ly[4951]
Thermodesulfatatorind
icus
55ndash80
(70)
60ndash
67(625)
H2C
O2stim
ulated
bymethano
lmon
omethylamine
glutam
atepepton
efumaratetryptone
isobu
tyrate3-C
H3
butyrateethanol
prop
anolandlow
amou
ntso
facetate
Sulfate
Marineh
ydrothermal
syste
mC
entralIndian
Ridge
[52]
Thermodesulfobacterium
hydrogeniphilum
50ndash80
(75)
63ndash68(65)
H2C
O2stim
ulated
byacetatefumarate
3-methylbutyrate
glutam
ateyeastextract
pepton
eortrypton
e
Sulfate
Marineh
ydrothermal
syste
mG
uaym
asBa
sin[53]
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
10 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Thermodesulfobacterium
commun
e41ndash83
60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA[5455]
Thermodesulfobacterium
thermophilum
nd60ndash
80(70)
H2C
O2pyruvate
lactate
Sulfatethiosulfate
nd[55]
Thermodesulfobacterium
hveragerdense
7545ndash70
(70)
H2pyruvatelactate
Sulfatesulfite
Hot
sprin
gs(m
icrobial
mats)Iceland
[56]
Thermodesulfobium
narugense
6940ndash
60(55ndash6
0)
H2C
O2
Sulfaten
itrate
thiosulfate
Hot
sprin
gs(m
icrobial
mats)Japan
[57]
Desulfotomaculum
spp(30
species)
nd23ndash55
H2C
O2formatesome
(organicacidslip
idsor
mon
oaromatic
hydrocarbo
ns)
Sulfidesulfur
thiosulfateA
cetate
some(Fe
(III)Mn(IV)
U(V
I)or
Cr(V
I))
Subsurface
environm
ents
rice
fieldsminesoilspills
[58ndash62]
Desulfosporosinus
meridiei
10ndash37
61ndash75
H2C
O2acetatesom
e(la
ctatepyruvate
ethano
l)Sulfatesom
e(nitrate)
Groun
dwater
contam
inated
with
polycyclica
romatic
hydrocarbo
nsinSw
anCoastalPlain
Australia
[63]
Desulfosporosinus
youn
gii
8ndash39
(32ndash35)
57ndash82(70ndash
73)
Beefextractyeast
extractform
ate
succinatelactate
pyruvateethanoland
toluene
Fumaratesulfatesulfite
thiosulfate
Artificialwetland
(sedim
ent)
[64]
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 11
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfosporosinus
orien
tis37ndash4
860ndash
65
H2C
O2formate
lactatepyruvatem
alate
fumaratesuccinate
methano
lethano
lprop
anolbutanol
butyratevalerate
palm
itate
Sulfatesulfite
thiosulfatesulfur
nd[65]
Desulfosporom
usapolytro
pa4ndash
3761ndash80
H2C
O2formate
lactatebu
tyrateseveral
alcoho
lsorganica
cids
carboh
ydratessome
aminoacidscholine
betaine
SulfateFe(OH) 3
Oligotroph
iclake
(sedim
ent)
German
[66]
Thermodesulfovibrio
yellowstonii
41ndash83
60ndash
80(70)
H2C
O2acetate
form
atelactate
pyruvate
Sulfatethiosulfate
sulfite
Hot
sprin
gs(w
ater
sedimentand
mats)
Yellowsto
neNational
ParkU
SA
[67]
Thermodesulfovibrio
islandicus
5545ndash70
(70)
H2pyruvatelactate
form
ate
Sulfaten
itrate
Bioreactor
inoculated
with
hotsprings
(microbialmats)sample
Iceland
[56]
Desulfohalobium
spp(6
species)
nd55ndash80(65ndash70)
H2lactateethanol
acetate
Sulfite
hypersaline
environm
ents
[6869]
Desulfocaldus
terraneus
58nd
H2C
O2aminoacids
proteinaceou
ssub
strates
andorganica
cids
prod
ucingethano
lacetateprop
ionate
isovalerate2-
methylbutyrate
Cystinesulfu
rsulfate
Seao
ilfacilitiesAlaksa
[70]
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
12 BioMed Research International
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfomicrobium
spp(4
species)
25ndash30
ndH2lactatepyruvate
Ethano
lform
ate
Sulfatesulfoxyanions
Anaerob
icsediments
(Freshwaterbrackish
marine)anaerob
icstrata
oroverlyingwaterand
insaturatedmineralor
organicd
eposits
[5469]
Desulfonatro
novibrio
hydrogenovoran
s37ndash4
090
ndash102(90ndash97)
H2formate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[71]
Desulfonatro
num
spp(3
species)
20ndash4
5(37ndash45)
80ndash
100(90)
H2form
ateYeast
extractethano
llactate
Sulfatesulfite
thiosulfate
Alkalines
odalakes
(anaerob
ic)
[72]
Desulfovibriospp(47
species)
25ndash4
4(25ndash35)
ndH2C
O2acetatelactate
carboh
ydrates
Sulfaten
itrate
nd[73]
Desulfomonile
spp(2
species)
30ndash30
(37)
65ndash78
(68ndash70)
H2C
O2benzoate
pyruvateorganic
carbon
halogens
Sulfatesulfite
thiosulfatesulfurFe
(III)NitrateU(V
I)Slud
ge[74]
Syntroph
obacteraceae
(8genera)
31ndash6
070
ndash75
H2C
O2acetate
form
atelactate
pyruvate
Sulfatesulfite
thiosulfate
Sewages
ludge
freshwaterbrackish
marines
edim
ent
marineh
ydrothermal
ventsho
tspring
sediments
[7375]
Desulfobacterium
anilini
3069ndash
75H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 13
Table2Con
tinued
Microorganism
Temperature
(∘ C)
pHa
Carbon
andele
ctron
source
Electro
nacceptor
Source
Reference
Desulfarculus
baarsii
35ndash39
73H2C
O2butyrate
high
erfatty
acidsother
organica
cidsalcoh
ols
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[76]
Desulfobacteraceae(12
genera)
10ndash4
0nd
H2C
O2L
ong-chain
fatty
acidsAlcoh
ols
Polara
romatic
compo
undsand
insome
casese
venAlip
hatic
arom
atichydrocarbo
ns
Sulfatesulfite
thiosulfate
Freshw
aterB
rackish
waterM
arineand
Haloalkalineh
abitats
[77]
Desulfosporosinus
acidophilus
25ndash4
036ndash
52(52)
H2lactatepyruvate
glycerolglucose
and
fructose
Sulfate
Sedimentfrom
anacid
effluent
pond
[26]
Desulfosporosinus
acididuran
s15ndash4
038ndash70
(55)
H2formatelactate
butyratefum
arate
malatepyruvate
glycerolm
ethano
lethano
lyeastextract
xyloseglucosefructose
Ferriciro
nnitrate
sulfateelem
entalsulfur
thiosulfate
Whiteriv
erdraining
from
theS
oufriere
hills
inMon
serrat(pH32)
[78]
a Valuesc
losedby
parenthesis
arec
onsid
ered
optim
alpH
ndno
tinformed
byconsultedreference
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
14 BioMed Research International
such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO
2[33]
In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO
2and H
2[17]
D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]
4 Natural Attenuation for the Design of AMDRemediation Strategies
Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and
chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH
2O)were detected presumably due
to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not
Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]
5 Concluding Remarks
Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools
Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes
Conflicts of Interest
The authors declare that there are no conflicts of interestregarding the publication of this paper
Acknowledgments
The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 15
(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)
References
[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013
[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014
[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012
[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008
[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011
[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003
[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000
[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014
[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006
[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005
[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007
[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008
[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008
[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015
[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013
[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006
[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006
[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014
[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008
[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006
[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010
[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005
[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016
[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999
[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001
[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010
[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990
[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016
[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014
[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009
[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
16 BioMed Research International
water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014
[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017
[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017
[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012
[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015
[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996
[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010
[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005
[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015
[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016
[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017
[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017
[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981
[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997
[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998
[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999
[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO
2fixation in Archaeoglobus lithotroph-
icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995
[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001
[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996
[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990
[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988
[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004
[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002
[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983
[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983
[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999
[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003
[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013
[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 17
sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006
[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997
[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005
[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011
[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001
[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009
[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985
[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004
[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994
[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991
[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009
[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997
[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998
[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015
[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015
[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014
[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987
[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980
[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015
[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012
[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992
[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011
[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007
[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Submit your manuscripts athttpswwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 201
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology