Review ArticlePhysical, Chemical, and Biological Methods for the Removal ofArsenic Compounds
K. T. Lim,1 M. Y. Shukor,1 and H. Wasoh2
1 Department of Biochemistry, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia (UPM),Serdang, 43400 Selangor, Malaysia
2 Department of Bioprocess Technology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia (UPM),Serdang, 43400 Selangor, Malaysia
Arsenic is a toxic metalloid which is widely distributed in nature. It is normally present as arsenate under oxic conditions whilearsenite is predominant under reducing condition. The major discharges of arsenic in the environment are mainly due to naturalsources such as aquifers and anthropogenic sources. It is known that arsenite salts are more toxic than arsenate as it binds withvicinal thiols in pyruvate dehydrogenase while arsenate inhibits the oxidative phosphorylation process. The common mechanismsfor arsenic detoxification are uptaken by phosphate transporters, aquaglyceroporins, and active extrusion system and reduced byarsenate reductases via dissimilatory reduction mechanism. Some species of autotrophic and heterotrophic microorganisms usearsenic oxyanions for their regeneration of energy. Certain species of microorganisms are able to use arsenate as their nutrientin respiratory process. Detoxification operons are a common form of arsenic resistance in microorganisms. Hence, the use ofbioremediation could be an effective and economic way to reduce this pollutant from the environment.
1. Introduction
Arsenic is one of the toxic metalloids that exists in more than200 differentmineral forms, where 60% of them are normallyarsenates; 20% are sulphosalts and sulphides; and the remain-ing 20% are arsenite, oxides, arsenide, silicates, and elementalarsenic [1, 2].The intrusion of orogenesis and graniticmagmahave resulted in the formation of arsenopyrite [1]. Arsenicwas first discovered by Albertus Magnus in the year 1250[3]. Under natural condition, arsenic normally cycled at theearth surface where the breakdown of rocks has convertedarsenic sulfides into arsenic trioxide [2, 4]. Furthermore,arsenic is known to have multiple oxidation states where theyare present in either organic or inorganic compounds in anaquatic environment [5, 6]. Both Zobrist et al. [7] and Root etal. [8] indicated that the mobility of arsenic inorganic com-pound in contaminated aquatic and sediment environmentis controlled by redox processes, precipitation, sorption, anddissolution processes. It is known that ferric iron phase playsan important role for the sorption of dissolved arsenate in
oxic groundwater [8]. Meanwhile, the reduction of arsenateinto arsenite in the transition from aerobic to anoxic porewaters is oftenmediated bymicrobial activity, which includesdetoxification and metabolic mechanisms [8]. In anotherstudy, Saalfield and Bostick [9] proposed that the presenceof calcium and bicarbonate from the byproducts of biologicalprocesses in the aquifers will enhance the release of arsenicand the correlations between calcium and bicarbonate witharsenic were then observed.
Arsenic usually exists in four oxidation states: As−3(arsine), As∘ (arsenic), As+3 (arsenite), and As+5 (arsenate)[4, 10]. In soil environment, arsenic is generally present in twooxidation states which are As+3 (arsenite) andAs+5 (arsenate)and normally present as amixture of As+3 (arsenite) andAs+5(arsenate) in air [2]. Of the two oxidation states, arsenate isthe main species associated with soil arsenic contaminations,and it is often written as AsO
4
3− which is very similar tophosphate [11, 12]. Arsenate could act as a potential oxidativephosphorylation inhibitor. This is a cause for concern since
Hindawi Publishing CorporationBioMed Research InternationalVolume 2014, Article ID 503784, 9 pageshttp://dx.doi.org/10.1155/2014/503784
2 BioMed Research International
oxidation phosphorylation is the main key reaction of energymetabolism in humans andmetazoans [4]. Arsenite has beenreported as the most toxic and soluble form of arsenic whencompared to arsenate, and it can bind with reactive sulfuratoms present in many enzymes, including enzymes whichare involved in respiration [4, 13]. Furthermore, it is knownthat soluble inorganic arsenic is often more toxic than theorganic form [2]. Unlike arsenate and arsenite, arsine is oftenavailable as highly toxic gases such as (CH
3
)3
and H3
As andoften present at low concentration in the environment [4].
Meanwhile, the average concentration of arsenic in freshwater is around 0.4𝜇g/L and could reach 2.6 𝜇g/L in seawater[13]. However, the thermal activity in some places has causedhigh level of arsenic in waters with the concentration ofarsenic in geothermal water in Japan ranging from 1.8to 6.4mg/L whereas the concentration of arsenic in NewZealand water could reach up to 8.5mg/L [2, 29, 30]. Inextreme cases, analysis from well drinking water in Jessore,Bangladesh, revealed that the levels of arsenic could reach upuntil 225mg/L [31]. On the other hand, the concentration ofarsenic in plants is solely depending on the amount of arsenicthat the plant is being exposed to where the concentration ofarsenic could range from less than 0.01 𝜇g/g (dried weight)in the uncontaminated area to around 5 𝜇g/g (dried weight)in the contaminated area [2]. Unlike plant, the concentrationof arsenic in marine organisms and mammals has a widerange of variations ranging from 0.005 to 0.3mg/kg in somecrustaceans and molluscs, 0.54 𝜇g/g in fish, over 100 𝜇g/gin some shellfish, and less than 0.3 𝜇g/g in humans anddomestic animals [2]. Presence of humic acid in the shallowsubsurface could affect the mobility of arsenic since humicacid could interact with aqueous arsenic for the formationof stable colloidal complexes that might play a prominentrole in the enhancement of arsenic mobility. Furthermore,the combination of humic acid together with ferric hydroxidesurface will lead to the formation of stable complexes thatwould compete with arsenic for its adsorption sites [32].
2. Usage of Arsenic
The first usage of arsenic in medicine could be dated around2500 years ago where it was mainly consumed for theimprovement of breathing problems as well as to give fresh-ness, beauty, and plumpness figures in women [2]. Arsenic inthe form of arsenical salvarsan (arsenic containing drug) wasthe initial antimicrobial agent used in the treatment of infec-tious diseases such as syphilis and sleeping sickness in 1908[3]. This drug was specifically developed by Sahachiro Hataunder the guidance of Paul Ehrlich in 1908 where they namedthe drug as arsphenamine no. 606 [33].Meanwhile, arsenic inthe form of arsenic trioxide (As
2
O3
) is one of the most com-mon forms of arsenic, which is often used in manufacturingand agriculture industry and for medical purposes such as inthe treatment of acute promyelocytic leukemia [34]. Arsenictrioxide is also proven to be useful in criminal homicidesdue to its characteristic, which is tasteless, colorless, highlytoxic, and soluble in water [2, 4]. The high usage of arsenictrioxide in suicide cases had made it to be often referred asthe “inheritance powder” in the 18th century [4].
During the 1970s, arsenic was mainly used in agricultureindustry in the form of insecticide’s component in order toget rid of the insects [2, 13, 35]. Arsenic was also used ascotton desiccants andwood preservatives inUnited States [2].The usage of arsenic as the cotton desiccant was introducedaround year 1956 and was widely used due to its effectivenessand affordable price [36]. Besides that, arsenic was also beingused in ceramic and glass industry, pharmaceutical industry,and food additives as well as pigments in paint [13, 34].Meanwhile, arsenic in the form of 4-aminoben-zenearsenicacid (p-arsenilic acid, p-ASA) has been used as animals foodadditive for feeding of boiler chickens [37].
3. Toxicity of Arsenic
It has been noticed that the extensive usage of arsenic in theindustrial and agrochemical applications is of few causesof groundwater and sediment arsenic contamination inthe environment [6, 38] in which effects are much smallercompared to the natural causes [39]. The presence of arsenicin soil and water has become an increasing problem in manycountries around the world, including Bangladesh, India,Chile, and Taiwan [2, 40, 41], and natural geological source isone of the main causes of contamination [34]. Consumptionof drinking water that has been contaminated by hazardouslevel of arsenic will lead to a wide range of diseases suchas arsenic dermatosis, lung cancer, liver cancer, uteruscancer, skin cancer and occurrence of skin, and bladder andhepatocellular carcinoma that will result in slow and painfuldeath [1, 2, 41–43]. In Southwestern Taiwan, the humanconsumption of artesian well waters which contains highconcentration of arsenic has also led to Blackfoot disease,which is an endemic peripheral vascular disease in that area[40]. In China, up to the year 2012, 19 provinces had beenfound to have As concentration in drinking water exceedingthe standard level (0.05mg/L). Inner Mongolia, Xinjiang,and Shanxi Provinces are historical well-known “hotspots”of geogenic As-contaminated drinking water [44].
Deltaic plain contaminated groundwater of Ganges-Meghna-Brahmaputra rivers in Bangladesh andWest Bengalhad resulted in an alarming environmental problem as thiswater is often consumed by people who live in that area[6, 45].The presence of aqueous arsenic is mainly due to rockweathering as well as sediment deposition and downstreamtransport of rich mineral arsenic that was originally presentin Himalayas [4]. Massive constructions of wells whichare meant to supply an improved quality of water withwaterborne pathogens free to the people living in this areahad created another problem as the ground water in thatarea was arsenic contaminated [4]. In Nepal, arsenic (As)contamination was a major issue in water supply drinkingsystems especially in high density population such as Teraidistricts. The local inhabitants still use hand tube and dugwells (with hand held pumps that are bored at shallow tomedium depth) for their daily water requirements [46]. Theresults of the analysis on 25,058 samples tested in 20 districts,published in the report of arsenic in Nepal, demonstratedthat 23% of the samples were containing 10–50 𝜇g/L ofAs, and 8% of the samples were containing more than
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50𝜇g/L of As. Recent status from over 737,009 samples testedhas shown that 7.9% and 2.3% were contaminated by 10–50𝜇g/L and >50𝜇g/L of As, respectively [46]. Other placesreporting the ground water arsenic contamination includesouthWest Coast of Taiwan; Antofagasta in Chile; six areas ofRegion Lagunera located in the central part of NorthMexico;Monte Quemado; Cordoba province in Argentina; MillardCounty in Utah, United States; Nova Scotia in Canada; andInner Mongolia, Qinghai, Jilin, Shanxi, Xinjiang Uygur A.R.,Ningxia, Liaoning, and Henan provinces in China [2].
Accidental ingestion of pesticides or insecticides con-taining arsenic will also result in an acute arsenic poisoningwhich sometimes could lead to mortality when 100mg to300mg of doses were being consumed [1]. The symptomsof acute arsenic poisoning are vomiting, abdominal pain,diarrhea, and cramping, which will then cause renal failure,haematological abnormalities such as leukemia and anemia,pulmonary oedema, and respiratory failure, and it couldfurther lead to shock, coma, and death [1, 2, 34]. In anotherstudy, Lai et al. [47] reported that the consumption of watercontaminated with arsenic will increase the risk of diabetesmellitus by twofold. In US, prevalence of diabetes increasedamong people having urine arsenic concentrations in morethan 20% of the general population [48]. Arsenic contamina-tion from industrial sources has also led to skinmanifestationof chronic arsenic poisoning, which affected 19.9% of thehuman populations living in Ron Phibun, Thailand [2]. Onthe other hand, arsenic poisoning caused by ingestion of food(especially seafood product) and beverages contaminated byarsenic has been reported in Japan, England, Germany, andChina [2]. In Campinas, Brazil, 116 samples of seafood (usedfor sashimi making) from Japanese restaurants have beenevaluated for the presence of As [49]. Several samples werefound with percentage above the maximum limit permittedby European regulations including 90% tuna, 48% salmon,31% mullet, and 100% octopus. It was concluded that theoctopus was the sashimi which most contributed to arsenic.In other case, the arsenic concentration in rice was found tobe high in Bangladesh [50].
Phosphate fertilization is suggested to lower the arsenateuptake in plants because both compounds enter the ricevia the same transporter. However, there are arguments incertain cases because under flooding conditions, As is presentas arsenite, which cannot compete with phosphate; further-more, phosphate increases As mobility because it competeswith arsenate for the adsorption site on Fe-oxides/hydroxides[51]. Presence of over 1.0𝜇g/g arsenic concentration in hair,20 to 130 𝜇g/g in nails, and over 100 𝜇g per day in urine isan indication of arsenic poisoning [2]. Significant correlationwas also observed with levels in human urine, toenail, andhair samples [31]. A meta-analysis assessing the effects ofexposure to arsenic suggests that 50% increment of arseniclevels in urine would be associated with 0.4 decrement inthe intelligence quotient (IQ) of children aged 5–15 years[52]. Arsenic uptake is adventitious because arsenate andarsenite are chemically similar to the required nutrients [53].At neutral pH, the trivalent forms of these metalloids arestructurally similar to glycerol, and hence they can enter cellsthrough aquaporins [54].
4. Technologies/Methods for the Removal ofArsenic from Environment
According to World Health Organisation (WHO) standardset in the year 1993, the maximum limit of arsenic con-tamination in drinking water is 10 𝜇g/L or 10 ppb. [1]. Thislimit was later adopted by European Union in the year1998 (council directive 98/83/EC), transposed by Portugueselegislation by Law Decree (DL) number 236/2001 [1, 55].In the year 2006, United States has also adopted the WHOstandard for lowering the federal drinking water standardfor maximum limit of arsenic from 50𝜇g/L to 10 𝜇g/L [8].Technologies for removing arsenic from the environmentshould meet several basic technical criteria that includerobustness, no other side effect on the environment, andthe ability to sustain water supply systems for long termsand meet the quality requirement of physical chemical, andmicrobiological approaches [1]. Currently, there are manymethods for removing arsenic from the soil contaminatedwith arsenic, which could be divided into three categories,including physical, chemical, and biological approaches [14].
In the physical approaches, the concentration of arsenic insoil could be reduced by mixture of both contaminated anduncontaminated soils together that will lead to an acceptablelevel of arsenic dilution [14]. Soil washing is another methodwhich is grouped under physical approaches whereby arseniccontaminated soil will bewashedwith different concentrationof chemicals such as sulfuric acid, nitric acid, phosphoricacid, and hydrogen bromide [14]. The choice of chemicalsused for extractant and high cost have often restricted theusage of soil washing into a smaller-scale operations asit is the disadvantages of using soil washing method [14].Meanwhile, cement can immobilise soluble arsenites and hasbeen successfully used to stabilise As-rich sludges which maybe suitable for treating sludges generated from precipita-tive removal units [15]. Furthermore, the disposal of watertreatment wastes containing As, with a particular emphasison stabilisation/solidification (S/S) technologies, has beenassessed for their appropriateness in treating As containingwastes. In this process, brine resulting from the regenerationof activated alumina filters is likely to accelerate cementhydration. Furthermore, additives (surfactants, cosolvents,etc.) have also been used to enhance the efficiencies ofsoil flushing using aqueous solutions as water solubility isthe controlling mechanism of contaminant dissolution. Theusage of surfactant alone gives about 80–85% of efficienciesin laboratory experiments. Studies indicated that when soilflushing is applied in the field, efficiency can vary from 0% toalmost 100%. It often givesmoderate efficiencies by using onlyone product (surfactant, cosolvent, and cyclodextrin). On theother hand, the use of more complex methods with polymerinjection leads to higher efficiencies [16].
The current available chemical remediation approachesmainly involving methods such as adsorption by usingspecific media, immobilization, modified coagulation alongwith filtration, precipitations, immobilizations, and complex-ation reactions [1, 14]. The coagulation along with filtrationmethod for removing arsenic from contaminated sources isquite economic but often displayed lower efficiencies (<90%)
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[1]. The formation of stable phases, for example, insolubleFeAsO
4
(and hydrous species of this compound such asscorodite, FeAsO
4
⋅2H2
O), is beneficial for the stabilizationprocedure [17]. Furthermore, the use of selective stabilizingamendments is a challenging task as the majority of pollutedsites are contaminated with multiple metal(loid)s. Nanosizedoxides and Fe(0) (particle size of 1 to 100 nm) are another pos-sible enhancement for the stabilization method [17]. Naturalnanoparticulate oxides are important scavengers of contami-nants in soils [56] and due to their reactive and relatively largespecific surface area (tens to hundreds m2/g), engineeredoxide nanoparticles are promising materials for the remedia-tion of soils contaminated with inorganic pollutants [18, 19].It is reported that chemical remediation gained popularitybecause of its high success rate, but it could be expensivewhen someone would like to remediate a large area [14]. Incontrast, biological remediation or bioremediation of soilscontaminatedwith either inorganic or organic arsenic presentin pesticides and hydrocarbons have been widely accepted insome places [14]. Even though bioremediation suffers severallimitations, these approaches have been gaining interest forthe remediation ofmetal(loid) contaminated soils due to theircost effectiveness [14]. Basically, bioremediation technologycould be divided into subcategories: intrinsic bioremediationand engineered bioremediation [14]. Intrinsic bioremediationis generally referred to as the degradation of arsenic bynaturally occurring microorganisms without intervention byhuman, and this method is more suitable for remediation ofsoil with a low level of contaminants [14]. Engineered biore-mediation often relies on intervention of human for optimiz-ing the environment conditions to promote the proliferationand activity of microorganisms that lived in that area. Asa result, the usage of engineered bioremediation method ismore favorable in the highly contaminated area [14].
Mechanism for arsenic detoxification can be divided intofour which known as uptake of As(V) in the form of arsenateby phosphate transporters, uptake of As(III) in the form ofarsenite by aquaglyceroporins, reduction of As(V) to As(III)by arsenate reductases, and extrusion or sequestration ofAs(III) [57]. AQPs have been shown to facilitate diffusion ofarsenic [53, 54]. The microbial oxidation of As in Altiplanobasins (rivers in northern Chile) was demonstrated by Leivaet al. [20]. The oxidation of As (As(III) to As(V)) is a criticaltransformation [58] because it favors the immobilizationof As in the solid phase. As(III) was actively oxidized bya microbial consortium, leading to a significant decreasein the dissolved As concentrations and a correspondingincrease in the sediment’s As concentration downstreamof the hydrothermal source. In situ oxidation experimentsdemonstrated that the As oxidation required a biologicalactivity, and microbiological molecular analysis had con-firmed the presence of As(III)-oxidizing groups (aro A-likegenes) in the system. In addition, the pH measurementsand solid phase analysis strongly suggest that As removalmechanism must involve adsorption or coprecipitation withFe-oxyhydroxides. Taken together, these results indicatedthat the microorganism-mediated As oxidation contributedto the attenuation of As concentrations and the stabilization
of As in the solid phase, therefore controlling the amountof As transported downstream [20]. Since most of thecases of arsenic poisoning are due to the consumption ofwater contaminated by arsenic, the process of cleaning upor reducing arsenic concentration in water becomes veryimportant. Methods used in reducing arsenic levels in waterare primarily divided into (i) physiochemicalmethods, whichinclude filtration or coagulation sedimentation, osmosis orelectrodialysis, adsorptions, and chemical precipitations and(ii) biological methods such as phytoremediation by usingaquatic plants or microbial detoxification of arsenic [14].
Generally, two approaches are mainly employed in thephytoremediation method. The first approach uses “free-floating plants such as water hyacinth” that could adsorbmetal(loid)s and the plants would be removed from thepond once the equilibrium state is achieved [14]. The secondapproach uses aquatic rooted plants (i.e., Agrostis sp., Pterisvittata, Pteris cretica, and others) to remove arsenic frombed filters and from water [14, 21–23]. Yang et al. [23] statedthat the addition of arsenate reducing bacteria will promotethe growth of P. vittata in soil. Two important processesin the removal of arsenic from water by microorganismsare biosorption and biomethylation [14]. It is reported thatbiomethylation (by As(III) S-adenosylmethionine methyl-transferase) is the reliable biological process for removingarsenic from aquatic media [14].
Recently, the arsenite (As(III)) S-adenosylmethioninemethyltransferase (ArsM) gene has been inserted into thechromosome of Pseudomonas putida KT2440 for potentialbioremediation of environmental arsenic [59].The first struc-ture of As(III) S-adenosylmethionine methyltransferase byX-ray crystallography was described by [60]. In this enzyme,there are three conserved cysteine residues at positions72, 174, and 224 in the CmArsM orthologue from thethermophilic eukaryotic alga Cyanidioschyzon sp. 5508 [61].Substitution of any of the three led to the loss of As(III)methylation [61]. The relationship between the arsenic andS-adenosylmethionine binding sites to a final resolution of∼1.6 A. As(III) binding causes little change in conformation,but binding of SAM reorients helix 𝛼4 and a loop (residues49–80) towards the As(III) binding domain, positioning themethyl group to be transfer to the metalloid [60].
5. Arsenic Resistant Microorganisms
Studies of bacterial growth at high arsenic-phosphorus ratiosdemonstrated that high arsenic concentrations can be toler-ated relatively and that it can be involved in vital functions inthe cell [62]. Corynebacterium glutamicum survives arsenicstress with two different classes of arsenate reductases.Cg-ArsC1 and Cg-ArsC2 are the single-cysteine monomericenzymes coupled to the mycothiol/mycoredoxin redoxpathway using amycothiol transferasemechanism, while Cg-ArsC1’ is a three-cysteine containing homodimer that usesa reduction mechanism linked to the thioredoxin pathway[63]. The presence of naturally occurring arsenate andarsenite in water and soil environment which could enter thecells by the phosphate-transport system has given pressurefor microorganisms to maintain their arsenic detoxification
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systems for surviving purposes. One of the commonest formsof arsenic resistance in microorganisms is by detoxificationoperons, which are encoded on genomes or plasmids [64].
Most of the detoxification operons consist of threegenes, which are known as arsC (reduction of arsenate toarsenite), arsR (transcriptional repressor), and arsB (can alsobe a subunit of the ArsAB As(III)-translocating ATPase,an ATP-driven efflux pump) [3, 53, 64]. Moreover, somedetoxification operons also contain two additional genes(arsD-metallochaperone and arsA-ATPase) [3, 64].TheArsDmetallochaperone binds cytosolic As(III) and transfers it tothe ArsA subunit of the efflux pump [53]. In normal process,arsenate that enters the cell will be reduced to arsenite byArsC gene before it is transported out of the cell by ArsBgene [10, 64]. As a result, a more toxic form of arsenicwill be introduced into the environment. In another study,Villegas-Torres et al. [65] indicated that the arsenic resistanceability in Bacillus sphaericus could be due to the presence ofarsC gene, which could be horizontally transferred betweenmicroorganisms isolated from Columbian oil polluted soilthat contain high arsenic levels.
The other reduction of arsenate to arsenite by microor-ganisms is via dissimilatory reduction mechanism that couldbe carried out in facultative anaerobe or strict anaerobecondition with the arsenate acting as the terminal electronacceptor [24]. These microorganisms have the ability tooxidize inorganic (sulfide and hydrogen) and organic (e.g.,formate, aromatics, and lactase acetate) as an electron donorwhich will lead to the production of arsenite, and they werenormally named dissimilatory arsenate-respiring prokary-otes (DARPs) [4].
Two other families of arsenate reductase are knownas thioredoxin (Trx) clade and Arr2p arsenate reductase.It is reported that Trx clade is linked with arsC arsenatereductase gene while Arr2p is related to different class oflarger protein tyrosine phosphatases [66]. Zargar et al. [67]reported that ArxA (arsenite oxidase) enzymes, which arepresent in Alkalilimnicola ehrlichiiMLHE-1 strain (a chemo-liautotroph bacteria) could couple with arsenite oxidationas well as nitrate reduction. Different types of bacteria withthe ability of resisting arsenic are Rhodococcus, Arthrobac-ter, Acinetobacter, Agrobacterium, Staphylococcus, Escherichiacoli, Thiobacillus, Achromobacter, Alcaligene, Pseudomonas,Microbacterium oxydans, Ochrobactrum anthropi, Cupri-avidus, Desulfomicrobium, Cyanobacteria, Sulfurospirillum,Wolinella, Citrobacter, Agrobacterium, an arsenic reducingbacteria from Flavobacterium-Cytophaga group, Scopulariop-sis koningii, Fomitopsis pinicola, Penicillium gladioli, Fusariumoxysporum meloni, Fucus gardneri, Bosea sp., Psychrobac-ter sp., Polyphysa peniculus, Methanobacterium, Bradyrhizo-bium, Rhodobium, Sinorhizobium, andClostridium [13, 21, 53,68–71].
Liao et al. [69] reported that 11 arsenic reducing bacteriastrains from seven different genera (i.e., Pseudomonas, Psy-chrobacter, Citrobacter, Bacillus, Bosea, Vibrio, and Enterobac-ter) were isolated from environmental groundwater samplescollected from well AG1 in Southern Yunlin County, west-central Taiwan. In Liao et al. [69] report, they indicated thatdiverse community of microorganisms holds a significant
impact in the biotransformation of arsenic that is presentin the aquifer, and these communities of bacteria are welladapted to high arsenic concentrations that are present in thewater. In another study, Mumford et al. [72] reported thatAlkaliphilus oremlandii and ferum reducing bacteria such asGeobacter species were present in arsenic rich groundwaterbeneath a site-specific site (C6) on Crosswicks Creek, NewJersey. Other bacteria with the ability of reducing arsenateto arsenite are Sulfurospirillum barnesii and Sulfurospirillumarsenophilum from the 𝜀-proteobacteria as well as Pyrobac-ulum arsenaticum from Thermoproteales order and Chrys-iogenes arsenatis [4, 10, 73, 74]. Afkar [10] reported that thereduction of arsenate to arsenite by S. barnesii strain SeS-3is associated with the membrane cell where this resistancemechanism is encoded by a single operon that consists ofarsenite ion-inducible repressor. Besides that, Afkar [10] alsoindicated that S. barnesii strain SeS-3 reduced arsenate toarsenite under anaerobic condition using arsenate as terminalelectron acceptors while lactate as the carbon source.
In another study, Youssef et al. [75] reported that bothNeisseria mucosa and Rahnella aquatilis are able to reducearsenate and selenate. In their study, both N. mucosa andR. aquatilis were grown in a neutral pH medium (pH 7)containing five mM sodium arsenates where the sodiumlactate acts as an electron donor while N. mucosa and R.aquatilis act as the electron acceptor organisms. Althoughboth N. mucosa and R. aquatilis strains studied are ableto grow at higher pH medium (pH10), their growth ratedecreased drastically (reduction of 43% in N. mucosa and67.2% in R. aquatilis) and has been observed [75]. Mean-while, archaebacterium Sulfolobus acidocaldarius strain BC,Alcaligenes faecalis, Shewanella algae, 𝛽-proteobacteria strainUPLAs1,Alcaligenes faecalis,Comamonas terrae sp. nov, someheterotrophic bacteria (Herminiimonas arsenicoxydans), andchemoliautotrophic bacteria are reported to have the abilityto oxidize arsenite to a less toxic arsenate [4, 14, 25–28]. Inthis case, arsenite will often serve as an electron donor forreducing the nitrate or oxygen that will produce energy inorder to fix carbon dioxide [26]. Two genes, aoxA and aoxBencoding for arsenite oxidase played an essential role in theoxidation of arsenite into arsenate [27].The insertion ofmini-Tn5::lacZ2 transposon in aoxA or aoxB gene will stop toarsenite oxidation process [27].
In another review by Silver and Phung [12], they indicatedthat both asoA and asoB genes which encoded for largemolybdopterin-containing and small Rieske (2Fe-2S) clusterthe subunit of oxidation of arsenite in Alcaligenes faecalis.They identified that the upstreams of asoB consist of 15genes while the downstreams of asoA consist of six genes,which are involved in arsenic resistance and metabolisms[12]. Besides bacteria, certain species of algae such as Fucusgardneri and Chlorella vulgaris are also known to have theability to accumulate arsenic [76, 77].
Table 1 shows the advantages and disadvantages of phys-ical, chemical, and biological methods for the removal ofarsenic compounds. Physical method exhibits the simplestchoice, but it was however limited to small scale operations.Chemical method had gained popularity by its high successrate; however, the remediation area can be exposed to other
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Table 1: Advantages and disadvantages of methods for the removal of arsenic compounds.
Method Method in detail Advantages/Disadvantages Reference
Physical approaches Mixing both contaminated and uncontaminatedsoils
High cost/usage to smaller-scaleoperations [14]
Physical approaches Washed with sulfuric acid, nitric acid, phosphoricacid, and hydrogen bromide
Physical approaches Immobilise soluble arsenites using cement Successfully used to stabilise As-richsludges [15]
Physical approaches Emphasis on stabilisation/solidification (S/S) Treating As containing wastes in water [15]
Physical approaches Soil flushing using aqueous solutions usingsurfactants and cosolvents
Applied in the field, efficiency can varyfrom 0% to almost 100% [16]
Chemical remediationapproaches
Adsorption by using specific media,immobilization, modified coagulation along withfiltration, precipitations, immobilizations, andcomplexation reactions
Economic but often displayed lowerefficiencies (<90%) [1, 14]
Chemical remediationapproaches
Formation of stable phases, for example, insolubleFeAsO4 (and hydrous species of this compoundsuch as scorodite, FeAsO4.2H2O)
Use of selective stabilizing amendments isa challenging task [17]
Chemical remediationapproaches
Stabilization method using nanosized oxides andFe(0) (particle size of 1 to 100 nm)
Gained popularity/high success rate, butit could be expensive when remediating alarge area
[14, 17–19]
Intrinsic bioremediation Degradation of arsenic by naturally occurringmicroorganisms
More suitable for remediation of soil witha low level of contaminants [14]
Engineered bioremediationOptimizing the environment conditions topromote the proliferation and activity ofmicroorganisms
Favorable method used in highcontaminated area [14]
Microbial oxidation Immobilization of As in the solid phase
Required biological activity, andmicrobiological molecularanalysis/involved adsorption orcoprecipitation with Fe-oxyhydroxides.
[20]
Physiochemical methodsFiltration or coagulation sedimentation, osmosisor electrodialysis, adsorptions, and chemicalprecipitations
Widely accepted in some places [14]
Biological methods Such as phytoremediation by using aquatic plantsor microbial detoxification of arsenic Widely accepted in some places [14]
Phytoremediation method Using “free-floating plants such as water hyacinth” Widely accepted in some places [14, 21–23]Using aquatic rooted plants such as Agrostis sp.,Pteris vittata, and Pteris cretica
Is a reliable biological process ofremoving arsenic from aquatic mediums [14]
ReductionReduction of arsenate into arsenite bymicroorganisms via dissimilatory reductionmechanism
Should be carried out in facultativeanaerobe or strict anaerobe condition [24]
OxidationUsing heterotrophic bacteria andchemoautotrophic bacteria to oxidize arseniteinto a less toxic arsenate
Should be carried out in controlledenvironment [4, 14, 25–28]
types of chemical contaminants. The usage of biologicaland phytoremediation methods might be the most practicalmethods for a small area but more research needs to becarried out especially in methylations, reduction, and oxi-dation using microorganisms for more effective method toremove the arsenic compound as they have a high potentialapplication in the future.
Previously, bacterial biosensors (whole-cell) were beingused to detect inorganic arsenic [78]. Biosensor technologywas widely studied by using potentiometry, amperometry,
and conductometry [79–81]. Only a few studies were carriedout based on capacitometry [82] especially by using DNAand antibodies [83, 84]. Previously, capacitive sensor usingenzyme was introduced for toxin detection [82]. A biosensorselective for the trivalent organoarsenicals methyl arsenateand phenyl arsenite over inorganic arsenite was reportedby Chen et al. [78] which may be useful for detectingdegradation of arsenic-containing herbicides and growthpromoters. A surface plasmon resonance biosensor for thestudy of trivalent arsenic was also reported by Liu et al. [85].
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This biosensor indicates that the 3D hydrogel-nanoparticlecoated sensors exhibited a higher sensitivity than that of the2D AuNPs decorated sensors. It was shown that bindingof As(III) into ArsA was greatly facilitated by the presenceof magnesium ion and ATP. For future research, biosensorbased on capacitometry using enzymes [82] such as As(III) S-adenosylmethionine methyltransferase for arsenic detectionremains interesting to be explored.
6. Conclusion
Arsenic is a metalloid that causes harm to humans andenvironments. However, certain species of prokaryotes havethe abilities to use arsenic either through oxidation orreduction process for energy conservation and growth pur-poses. It is important to remove and reduce this pollutantfrom the environment through different approaches such asphysical, chemical, and biological. The use of bioremediationto remove and mobilize arsenic from contaminated soils andaquifers could be an effective and economic way since a widerange of microorganisms have been found to be successfullydegrading this pollutant from the environment.
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper.
References
[1] A. A. L. S. Duarte, S. J. A. Cardoso, and A. J. Alcada, “Emergingand innovative techniques for arsenic removal applied to a smallwater supply system,” Sustainability, vol. 1, pp. 1288–1304, 2009.
[2] B. K. Mandal and K. T. Suzuki, “Arsenic round the world: areview,” Talanta, vol. 58, no. 1, pp. 201–235, 2002.
[3] B. P. Rosen, “Families of arsenic transporters,” Trends in Micro-biology, vol. 7, no. 5, pp. 207–212, 1999.
[4] R. S. Oremland and J. F. Stolz, “Arsenic, microbes and contami-nated aquifers,” Trends in Microbiology, vol. 13, no. 2, pp. 45–49,2005.
[5] J. G. Sanders, “Arsenic cycling in marine systems,”Marine Envi-ronmental Research, vol. 3, no. 4, pp. 257–266, 1980.
[6] S. M. Tareq, S. Safiullah, H. M. Anawar, M. M. Rahman, and T.Ishizuka, “Arsenic pollution in groundwater: a self-organizingcomplex geochemical process in the deltaic sedimentary envi-ronment, Bangladesh,” Science of the Total Environment, vol. 313,no. 1–3, pp. 213–226, 2003.
[7] J. Zobrist, P. R. Dowdle, J. A. Davis, andR. S. Oremland, “Micro-bial arsenate reduction vs arsenate sorption: experiments withferrihydrite suspensions,”MinerologicalMagazine A, vol. 62, pp.1707–1708, 1998.
[8] R. A. Root, D. Vlassopoulos, N. A. Rivera, M. T. Rafferty, C.Andrews, and P. A. O’Day, “Speciation and natural attenuationof arsenic and iron in a tidally influenced shallow aquifer,”Geochimica et Cosmochimica Acta, vol. 73, no. 19, pp. 5528–5553,2009.
[9] S. L. Saalfield and B. C. Bostick, “Synergistic effect of calciumand bicarbonate in enhancing arsenate release from ferrihy-drite,” Geochimica et Cosmochimica Acta, vol. 74, no. 18, pp.5171–5186, 2010.
[10] E. Afkar, “Localization of the dissimilatory arsenate reductasein Sulfurospirillum barnesii strain SeS-3,” American Journal ofAgriculture and Biological Sciences, vol. 7, pp. 97–105, 2012.
[11] J. F. Artiola, D. Zabcik, and S. H. Johnson, “In situ treatmentof arsenic contaminated soil from a hazardous industrial site:laboratory studies,”Waste Management, vol. 10, no. 1, pp. 73–78,1990.
[12] S. Silver and L. T. Phung, “Genes and enzymes involved inbacterial oxidation and reduction of inorganic arsenic,” Appliedand Environmental Microbiology, vol. 71, no. 2, pp. 599–608,2005.
[13] C. Cervantes, G. Ji, J. L. Ramırez, and S. Silver, “Resistanceto arsenic compounds in microorganisms,” FEMSMicrobiologyReviews, vol. 15, no. 4, pp. 355–367, 1994.
[14] S. Mahimairaja, N. S. Bolan, D. C. Adriano, and B. Robinson,“Arsenic contamination and its risk management in complexenvironmental settings,” Advances in Agronomy, vol. 86, pp. 1–82, 2005.
[15] C. Sullivan, M. Tyrer, C. R. Cheeseman, and N. J. D. Graham,“Disposal of water treatment wastes containing arsenic—areview,” Science of the Total Environment, vol. 408, no. 8, pp.1770–1778, 2010.
[16] O.Atteia, E.D. C. Estrada, andH. Bertin, “Soil flushing: a reviewof the origin of efficiency variability,” Review of Environment,Science and Biotechnology, vol. 12, pp. 379–389, 2013.
[17] M. Komarek, A. Vanek, and V. Ettler, “Chemical stabilizationof metals and arsenic in contaminated soils using oxides,” Envi-ronmental Pollution, vol. 172, pp. 9–22, 2013.
[18] N. C. Mueller and B. Nowack, “Nanoparticles for remediation:solving big problems with little particles,” Elements, vol. 6, no.6, pp. 395–400, 2010.
[19] K.-R. Kim, B.-T. Lee, and K.-W. Kim, “Arsenic stabilization inmine tailings using nano-sized magnetite and zero valent ironwith the enhancement of mobility by surface coating,” Journalof Geochemical Exploration, vol. 113, pp. 124–129, 2012.
[20] E. D. Leiva, C. D. P. Ramila, I. T. Vargas et al., “Naturalattenuation process via microbial oxidation of arsenic in a highAndean watershed,” Science of the Total Environment, vol. 466-467, pp. 490–502, 2014.
[21] E. K. Porter and P. J. Peterson, “Arsenic accumulation byplants on mine waste (United Kingdom),” Science of the TotalEnvironment, vol. 4, no. 4, pp. 365–371, 1975.
[22] M. I. Silva Gonzaga, J. A. Gonzaga Santos, and L. Q. Ma,“Arsenic phytoextraction and hyperaccumulation by fern spe-cies,” Scientia Agricola, vol. 63, no. 1, pp. 90–101, 2006.
[23] Q. Yang, S. Tu, G. Wang, X. Liao, and X. Yan, “Effectiveness ofapplying arsenate reducing bacteria to enhance arsenic removalfrom polluted soils by Pteris vittata L,” International Journal ofPhytoremediation, vol. 14, no. 1, pp. 89–99, 2012.
[24] J. Xiong, W. Wang, H. Fan, L. Cai, and G. Wang, “Arsenicresistant bacteria in mining wastes from Shangrao coal mine ofChina,” Environmental Science and Technology, vol. 1, pp. 535–540, 2006.
[25] H. M. Sehlin and E. B. Lindstrom, “Oxidation and reduction ofarsenic by Sulfolobus acidocaldarius strain BC,” FEMS Microbi-ology Letters, vol. 93, no. 1, pp. 87–92, 1992.
[26] D. Lievremont, P. N. Bertin, andM.-C. Lett, “Arsenic in contam-inated waters: biogeochemical cycle, microbial metabolism andbiotreatment processes,”Biochimie, vol. 91, no. 10, pp. 1229–1237,2009.
8 BioMed Research International
[27] D. Muller, D. Lievremont, D. D. Simeonova, J.-C. Hubert, andM.-C. Lett, “Arsenite oxidase aox genes from a metal-resistant𝛽-proteobacterium,” Journal of Bacteriology, vol. 185, no. 1, pp.135–141, 2003.
[28] K. Chitpirom, S. Tanasupawat, A. Akaracharanya et al., “Coma-monas terrae sp. nov., an arsenite-oxidizing bacterium isolatedfrom agricultural soil in Thailand,” Journal of General andApplied Microbiology, vol. 58, pp. 245–251, 2012.
[29] J. A. Ritchie, “Arsenic and antimony in New Zealand thermalwaters,”NewZealand Journal of Science, vol. 4, pp. 218–229, 1961.
[30] H. Nakahara, M. Yanokura, and Y. Murakami, “Environmentaleffects of geothermal waste water on the near-by river system,”Journal of Radioanalytical Chemistry, vol. 45, no. 1, pp. 25–36,1978.
[31] M. Kato, M. Y. Kumasaka, S. Ohnuma et al., “Comparison ofbariumand arsenic concentrations inwell drinkingwater and inhuman body samples and a novel remediation system for theseelements inwell drinkingwater,”PLoSONE, vol. 8, pp. 1–6, 2013.
[32] E. D. Burton, S. G. Johnston, and B. Planer-Freidrich, “Couplingof arsenic mobility to sulfur transformations during microbialsulfate reduction in the presence and absence of humic acid,”Chemical Geology, vol. 343, pp. 12–24, 2013.
[33] Sahachiro Hata, “The first miracle medicine in the worldfor syphilis treatment,” The World’s Greatest Japanese,2008, http://www.japanese-greatest.com/biology-medicine/sahachiro-hata.html.
[34] R. N. Ratnaike, “Acute and chronic arsenic toxicity,” Postgradu-ate Medical Journal, vol. 79, no. 933, pp. 391–396, 2003.
[35] O. Spiegelstein, A. Gould, B.Wlodarczyk et al., “Developmentalconsequences of in utero sodium arsenate exposure in micewith folate transport deficiencies,” Toxicology and Applied Phar-macology, vol. 203, no. 1, pp. 18–26, 2005.
[36] S. Crawford, J. T. Cothren, D. E. Sohan, and J. R. Supak, “Ahistory of cotton harvest AIDS,” inCottonHarvestManagement:Use and Influence of Harvest Aids, J. R. Supak and C. E. Snipes,Eds., pp. 1–19, The Cotton Foundation, Cordova Memphis,Tenn, USA, 2001.
[37] B. P. Jackson andP.M. Bertsch, “Determination of arsenic speci-ation in poultry wastes by IC-ICP-MS,” Environmental Scienceand Technology, vol. 35, no. 24, pp. 4868–4873, 2001.
[38] N. E. Keon, C. H. Swartz, D. J. Brabander, C. Harvey, andH. F. Hemond, “Validation of an arsenic sequential extractionmethod for evaluating mobility in sediments,” EnvironmentalScience and Technology, vol. 35, no. 13, pp. 2778–2784, 2001.
[39] O. Mondal, S. Bhowmick, D. Chatterjee, A. Figoli, and B. V.der Bruggen, “Remediation of inorganic arsenic in groundwaterfor safe water supply: a critical assessment of technologicalsolutions,” Chemosphere, vol. 92, pp. 157–170, 2013.
[40] C.-H. Tseng, “Blackfoot disease and arsenic: a never-endingstory,” Journal of Environmental Science and Health C, vol. 23,no. 1, pp. 55–74, 2005.
[41] A. Hadi and R. Parveen, “Arsenicosis in Bangladesh: prevalenceand socio-economic correlates,” Public Health, vol. 118, no. 8, pp.559–564, 2004.
[42] N. K. Mandal and R. Biswas, “A study on arsenical dermatosisin rural community of West Bengal,” Indian Journal of PublicHealth, vol. 48, no. 1, pp. 30–33, 2004.
[43] S.-N. Lu, N.-H. Chow, W.-C. Wu et al., “Characteristics ofhepatocellular carcinoma in a high arsenicism area in taiwan: acase-control study,” Journal of Occupational and EnvironmentalMedicine, vol. 46, no. 5, pp. 437–441, 2004.
[44] J. He and L. Charlet, “A review of arsenic presence in Chinadrinking water,” Journal of Hydrology, vol. 492, pp. 79–88, 2013.
[45] R. Nickson, J. McArthur, W. Burgess, K. Matin Ahmed, P.Ravenscroft, andM.Rahman, “Arsenic poisoning of Bangladeshgroundwater,” Nature, vol. 395, no. 6700, p. 338, 1998.
[46] J. K.Thakur, R. K.Thakur, A. L. Ramanathan, M. Kumar, and S.K. Singh, “Arsenic contamination of groundwater in Nepal-Anoverview,”Water, vol. 3, pp. 1–20, 2011.
[47] M.-S. Lai, Y.-M. Hsueh, C.-J. Chen et al., “Ingested inorganicarsenic and prevalence of diabetes mellitus,” American Journalof Epidemiology, vol. 139, no. 5, pp. 484–492, 1994.
[48] E. A. Maull, H. Ahsan, J. Edwards, M. P. Longnecker, A. Navas-Acien, and J. Pi, “Evaluation of the association between arsenicand diabetes: a national toxicology program workshop review,”Environmental Health Perspectives, vol. 120, pp. 1658–1670, 2012.
[49] M. A.Morgano, L. C. Rabonato, R. F. Milani, L. Miyagusku, andK. D. Quintaes, “As, Cd, Cr, Pb and Hg in seafood species usedfor sashimi and evaluation of dietary exposure,” Food Control,vol. 36, pp. 24–29, 2014.
[50] R. Y. Li, J. L. Stroud, J. F. Ma, S. P. Mcgrath, and F. J.Zhao, “Mitigation of arsenic accumulation in rice with watermanagement and silicon fertilization,” Environmental Scienceand Technology, vol. 43, no. 10, pp. 3778–3783, 2009.
[51] P. K. Sahoo and K. Kim, “A review of the arsenic concentrationin paddy rice from the perspective of geoscience,” GeosciencesJournal, vol. 17, pp. 107–122, 2013.
[52] M. Rodrıguez-Barranco, M. Lacasana, C. Aguilar-Garduno etal., “Association of arsenic, cadmium and manganese exposurewith neurodevelopment and behavioural disorders in children:a systematic review and meta-analysis,” Science of the TotalEnvironment, vol. 454, pp. 562–577, 2013.
[53] H. C. Yang, H. L. Fu, Y. F. Lin, and B. P. Rosen, “Pathways ofarsenic uptake and efflux,” Current Topics in Membranes, vol.69, pp. 325–358, 2012.
[54] B. P. Rosen and M. J. Tamas, “Arsenic transport in prokaryotesand eukaryotic microbes,” Advances in Experimental Medicineand Biology, vol. 679, pp. 47–55, 2010.
[55] Council Directive 98/83/EC, “The quality of water intendedfor human consumption,” Official Journal of the EuropeanCommunities, vol. 330, pp. 32–54, 1998.
[56] G. A.Waychunas, C. S. Kim, and J. F. Banfield, “Nanoparticulateiron oxide minerals in soils and sediments: unique propertiesand contaminant scavenging mechanisms,” Journal of Nanopar-ticle Research, vol. 7, no. 4-5, pp. 409–433, 2005.
[57] B. P. Rosen, “Biochemistry of arsenic detoxification,” FEBSLetters, vol. 529, no. 1, pp. 86–92, 2002.
[58] R. Mukhopadhyay, B. P. Rosen, L. T. Phung, and S. Silver,“Microbial arsenic: from geocycles to genes and enzymes,”FEMS Microbiology Reviews, vol. 26, no. 3, pp. 311–325, 2002.
[59] J. Chen, J. Qin, Y. G. Zhu, V. de Lorenzo, and B. P. Rosen, “Engi-neering the soil bacterium pseudomonas putida for arsenicmethylation,” Applied and Environmental Microbiology, vol. 79,pp. 4493–4495, 2013.
[60] A. A. Ajees, K. Marapakala, C. Packianathan, B. Sankaran, andB. P. Rosen, “Structure of an As(III) S-adenosylmethioninemethyltransferase: insights into the mechanism of arsenicbiotransformation,” Biochemistry, vol. 51, pp. 5476–5485, 2012.
[61] B. Rosen, K. Marapakala, A. A. Abdul Salam, C. Packianathan,and M. Yoshinaga, “Pathways of arsenic biotransformations:the arsenic methylation cycle,” in Understanding the Geologicaland Medical Interface of Arsenic, 4th International Congress onArsenic in the Environment, pp. 185–188, 2012.
BioMed Research International 9
[62] B. P. Rosen, A. A. Ajees, and T. R. Mcdermott, “Life and deathwith arsenic,” BioEssays, vol. 33, no. 5, pp. 350–357, 2011.
[63] L. M. Mateos, B. Rosen, and J. Messens, “The arsenic stressdefense mechanism of Corynebaterium glutamicum revealed,”inUnderstanding theGeological andMedical Interface of Arsenic,4th International Congress on Arsenic in the Environment, pp.209–210, 2012.
[64] W.Musingarimi, M. Tuffin, and D. Cowan, “Characterisation ofthe arsenic resistance genes in Bacillus sp. UWC isolated frommaturing fly ash acid mine drainage Neutralised solids,” SouthAfrican Journal of Science, vol. 106, no. 1-2, pp. 59–63, 2010.
[65] M. F. Villegas-Torres, O. C. Bedoya-Reina, C. Salazar, M. J.Vives-Florez, and J. Dussan, “Horizontal arsC gene transferamong microorganisms isolated from arsenic polluted soil,”International Biodeterioration and Biodegradation, vol. 65, no.1, pp. 147–152, 2011.
[66] R. Mukhopadhyay and P. R. Barry, “Arsenate reductases inprokaryotes and eukaryotes,” Environmental Health Perspec-tives, vol. 10, no. 5, pp. 745–748, 2002.
[67] K. Zargar, S. Hoeft, R. Oremland, and C. W. Saltikov, “Identi-fication of a novel arsenite oxidase gene, arxA, in the haloal-kaliphilic, arsenite-oxidizing bacteriumAlkalilimnicola ehrlichiistrain MLHE-1,” Journal of Bacteriology, vol. 192, no. 14, pp.3755–3762, 2010.
[68] J. F. Stolz and R. S. Oremland, “Bacterial respiration of arsenicand selenium,” FEMS Microbiology Reviews, vol. 23, no. 5, pp.615–627, 1999.
[69] V. H.-C. Liao, Y.-J. Chu, Y.-C. Su et al., “Arsenite-oxidizingand arsenate-reducing bacteria associated with arsenic-richgroundwater in Taiwan,” Journal of ContaminantHydrology, vol.123, no. 1-2, pp. 20–29, 2011.
[70] S. Honschopp, N. Brunken, A. Nehrkorn, and H. J. Breunig,“Isolation and characterization of a new arsenic methylatingbacterium from soil,”Microbiological Research, vol. 151, no. 1, pp.37–41, 1996.
[71] P. Aksornchu, P. Prasertsan, and V. Sobhon, “Isolation ofarsenic-tolerant bacteria from arsenic-contaminated soil,”Songklanakarin Journal of Science and Technology, vol. 30, no.1, pp. 95–102, 2008.
[72] A. C.Mumford, J. L. Barringer,W.M. Benzel, P. A. Reilly, and L.Y. Young, “Microbial transformations of arsenic: mobilizationfrom glauconitic sediments to water,” Water Research, vol. 46,no. 9, pp. 2859–2868, 2012.
[73] R. Huber, M. Sacher, A. Vollmann, H. Huber, and D. Rose,“Respiration of arsenate and selenate by hyperthermophilicarchaea,” Systematic and Applied Microbiology, vol. 23, no. 3, pp.305–314, 2000.
[74] R. S. Oremland and J. F. Stolz, “The ecology of arsenic,” Science,vol. 300, no. 5621, pp. 939–944, 2003.
[75] G. A. Youssef, S. A. El-Aassar, M. Berekaa, M. El-Shaer, andJ. Stolz, “Arsenate and selenate reduction by some facultativebacteria in the Nile Delta,” American-Eurasian Journal of Agri-culture and Environmental Science, vol. 5, pp. 847–855, 2009.
[76] S. C. R. Granchinho, E. Polishchuk, W. R. Cullen, and K. J.Reimer, “Biomethylation and bioaccumulation of arsenic(V) bymarine alga Fucus gardneri,”Applied Organometallic Chemistry,vol. 15, no. 6, pp. 553–560, 2001.
[77] S. Maeda, S. Nakashima, T. Takeshita, and S. Higashi, “Bioac-cumulation of arsenic by freshwater algae and the applicationto the removal of inorganic arsenic from an aqueous phase.Part II. By Chlorella vulgaris isolated from arsenic-polluted
environment,” Separation Science and Technology, vol. 20, no.2-3, pp. 153–161, 1985.
[78] J. Chen, Y. G. Zhu, and B. P. Rosen, “A novel biosensor selectivefor organoarsenicals,”Applied and Environmental Microbiology,vol. 78, pp. 7145–7147, 2012.
[79] W. Ngeontae, W. Janrungroatsakul, P. Maneewattanapinyo,S. Ekgasit, W. Aeungmaitrepirom, and T. Tuntulani, “Novelpotentiometric approach in glucose biosensor using silvernanoparticles as redoxmarker,” Sensors andActuators B, vol. 137,no. 1, pp. 320–326, 2009.
[80] Y. Zhou and J. Zhi, “The application of boron-doped diamondelectrodes in amperometric biosensors,” Talanta, vol. 79, no. 5,pp. 1189–1196, 2009.
[81] Z.Gao andN.Tansil, “ADNAbiosensor based on the electrocat-alytic oxidation of amine by a threading intercalator,” AnalyticaChimica Acta, vol. 636, no. 1, pp. 77–82, 2009.
[82] H. Wasoh, L. Y. Heng, F. Abu Bakar et al., “A simple capacitivebiosensor device for histamine measurement,” Sensor Review,vol. 32, pp. 245–250, 2012.
[83] L. Malic, T. Veres, and M. Tabrizian, “Biochip functional-ization using electrowetting-on-dielectric digital microfluidicsfor surface plasmon resonance imaging detection of DNAhybridization,” Biosensors and Bioelectronics, vol. 24, no. 7, pp.2218–2224, 2009.
[84] R. Hao, D. Wang, X. Zhang et al., “Rapid detection of Bacil-lusanthracis using monoclonal antibody functionalized QCMsensor,” Biosensors and Bioelectronics, vol. 24, no. 5, pp. 1330–1335, 2009.
[85] C. Liu,V. Balsamo,D. Sun et al., “A 3D localized surface plasmonresonance biosensor for the study of trivalent arsenic binding tothe ArsA ATPase,” Biosensors and Bioelectronics, vol. 38, pp. 19–26, 2012.
