Articulo 20 Mayo Extremophiles From Abyssal to Terrestrial Ecosystems and Possibly...

REVIEW

Extremophiles: from abyssal to terrestrial ecosystemsand possibly beyond

Francesco Canganella & Juergen Wiegel

Received: 7 May 2010 /Revised: 17 February 2011 /Accepted: 18 February 2011 /Published online: 11 March 2011# Springer-Verlag 2011

Abstract The anthropocentric term extremophile wasintroduced more than 30 years ago to describe anyorganism capable of living and growing under extremeconditionsi.e., particularly hostile to human and to themajority of the known microorganisms as far as tempera-ture, pH, and salinity parameters are concerned. With thefurther development of studies on microbial ecology andtaxonomy, more extreme environments were found andmore extremophiles were described. Today, many differentextremophiles have been isolated from habitats characterizedby hydrostatic pressure, aridity, radiations, elevatedtemperatures, extreme pH values, high salt concentra-tions, and high solvent/metal concentrations, and it iswell documented that these microorganisms are capableof thriving under extreme conditions better than anyother organism living on Earth. Extremophiles have alsobeen investigated as far as the search for life in otherplanets is concerned and even to evaluate the hypothesisthat life on Earth came originally from space. Extremophilesare interesting for basic and applied sciences. Particularlyfascinating are their structural and physiological featuresallowing them to stand extremely selective environmentalconditions. These properties are often due to specificbiomolecules (DNA, lipids, enzymes, osmolites, etc.) that

have been studied for years as novel sources for biotechno-logical applications. In some cases (DNA polymerase,thermostable enzymes), the search was successful and thefinal application was achieved, but certainly further exploita-tions are next to come.

Keywords Extremophilic microorganisms . Extremeenvironments . Taxonomy . Physiology . Application

Introduction

The majority of higher organisms live under conventionalconditions, that is, they grow and thrive under conditions ofmoderate temperature, pH, salinity, water availability,oxygen levels, pressure, and carbon and energy availability.These parameters, i.e., what defines moderate, are anthro-pocentric, clustering around temperature 37 C, pH 7.4,salinity from 0.9% to 3%, and 1 atm pressure and representthe ideal conditions for growing Escherichia coli as well asthose conditions which are comfortable for human beings.Formerly, these conditions were referred to as normal orphysiologic, but particularly over the last century,exploration of other environments has shown that a largenumber of organisms live under, or actually require, moreextreme conditions, i.e., conditions hostile to humans andmost of their microbial commensals (Grant 1988; Aguilar1996; Aguilar et al. 1998; Antranikian et al. 2005).

MacElroy coined the term extremophile in 1974 todescribe these organisms, and while containing some proto-zoal, algal, and fungal species, the majority of extremophilesare prokaryotic (MacElroy 1974). As conditions becomemore demanding, extreme environments become exclusivelypopulated by prokaryotes (Horikoshi 1998). While im-proved or more avid culture techniques are responsible for

F. Canganella (*)Department of Agrobiology and Agrochemistry,University of Tuscia,Via C. de Lellis,01100 Viterbo, Italye-mail: [email protected]

J. WiegelDepartment of Microbiology and Center for Biological ResourceRecovery, University of Georgia,215 Biological Sciences Building,Athens, GA 30601, USA

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the isolation of some of these species, the initiative to lookinto environments formerly considered uninhabitable, andthe development of technology necessary for these activities,has allowed isolation of many more. Any environment islikely to contain living organismsone just has to knowhow to recognize their presence. One example of this is theDead Sea, thought to be lifeless, but actually containingquite a variety of exciting prokaryotic (Arahal et al. 2000)and even eukaryotic (Buchalo et al. 1998) life forms.

Aside from intellectual curiosity, interest in studyingextremophiles stems from their possible utility in industrialprocesses, their possible links to the origins of life on thisplanet, and possible clues as to how and where to look forextraterrestrial life (Stetter 1996; Shock 1997; Litchfield1998; Wiegel and Adams 1998; Javaux 2006; Lentzen andSchwarz 2006; Villar and Edwards 2006). Some examplesof industrial applications of extremophiles are shown inTable 1.

Extremophiles may be divided into two broad categories:true (obligate) extremophiles which require one or moreextreme conditions in order to grow and multiply andfacultative extremophiles which can tolerate quite wellconditions which are toxic and/or lethal to the overwhelming

majority of living organisms, though growing optimally atnormal conditions. Presently, some orders or genera containonly extremophiles, whereas other orders or genera containboth extremophiles and non-extremophiles; however, withconstantly novel organisms identified and the assumptionsthat we have identified less than 2% of the assumed existingmicroorganisms, this divisionmay change frequently. In somecases, it is assumed that extremophiles are phylogeneticallythe older ones (e.g., thermophilic Clostridia), whereas inother instances, the extremophiles are assumed to besecondary adaptations (Wiegel and Adams 1998).Extremophiles are best characterized by the minimum,maximum, and optimum parameters of the extreme conditionfor growth, i.e., the Tmin, Topt, and Tmax for thermophiles.This review will discuss the various categories ofextremophilic prokaryotes and explore their habitats, bio-chemistry, interesting cellular processes or products, andpossible scientific and practical uses. Of course morpho-logical investigations have always been important issues as faras the characterization of extremophiles is concerned (Fig. 1),but they will not be discussed here; the same for the specificdescription of different extreme environments (examples inFigs. 2 and 3) that will be mentioned but not in detail.

Table 1 Biotechnological applications of major groups of extremophiles

Extremophilic organisms Enzymes and organiccompounds

Applications and products

Thermophiles and hyperthermophiles (Topt 55105 C) Amylases Glucose, fructose for sweeteners

Xylanases Paper bleaching

Proteases Amino acid production from keratins, food processing,baking, brewing, detergents

DNA polymerases Genetic engineering

Psychrophiles and psychrotolerants (Topt

Extremes of temperature

Mesophiles usually thrive in a temperature range of about710 C to 3542 C, with thermophiles and psychrophilesgrowing optimally in higher and lower temperature ranges,respectively. An organism is classified as tolerant to

extreme temperatures if it has its temperature optimum forgrowth in the mesophilic range but is able to grow andmultiply in extreme temperatures as well and considered-philic if it requires the elevated or lowered tempera-ture to grow and divide, with the optimal and maximalcardinal temperature parameters outside the mesophilicrange. For example, a bacterium which is able to growat 60 C, but also able to grow at 30 C, with an optimum at37 C, should be considered thermotolerant, while a bacteriumwhich grows optimally at 60 C, but not below 45 C, and

a

b

c

Fig. 1 Electromicroscopic pictures showing different extremophilesthat have been studied in environment at elevated temperatures: aThermococcus guaymasensis, b Clostridium thermobutyricum, csyntrophic bacteria of Riftia pachiptylia (courtesy by CM Cavanaugh).Scale bar 1 m

a

b

c

Fig. 2 Some environments where extremophiles can be isolated: a apower plant in Iceland, b the salt desert of Atacama (Chile), c deep-sea hydrothermal vents at Okinawa Trough (Japan)

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with a maximum temperature approximately 70 C is athermophile. For organisms which grow optimally in thethermophilic range, e.g., Topt=65

C, but have extendedtemperature ranges for growth below 45 C, e.g., Tmin=3 C(i.e., exhibiting a temperature span for growth of 35 C ormore), Wiegel has coined the term temperature-tolerantthermophile (Wiegel 1990). Extreme thermophiles are thoseable to grow above 70 C and have a Topt above 60 C,whereas hyperthermophiles have a Topt at and above 80 Cand frequently can grow above 100 C; the highesttemperature maximum so far observed is 121 C. The termsobligate psychrophile or obligate thermophile are some-times used, but are actually redundant.

Biotechnological applications of psychrophiles andpsychrotolerant organisms were mainly focused onenzymes, which include detergent additives for cold waterwashing (more eco-friendly and accessible than hot waterwashing) and cellulases for fabric processing, such asreducing pilling of garments. The cold-adapted enzymesexcise protruding cotton fiber ends from garments withoutdecreasing the strength and durability of the garmentbecause they are less resistant to subsequent inactivationthan currently used enzymes (Gerday et al. 1997; Evangelistaet al. 2009; Matsuo et al. 2010). Cold-adapted enzymes areuseful in the food industry for food modifications (Sproessler1993) and in bioremediation (Margesin and Schinner 1998;Lettinga et al. 1999).

Thermophiles are also interesting from the viewpoint ofthe trend toward biotechnologymany chemical industrial

processes employ high temperatures, which would have tobe lowered in order to use bioprocesses from mesophiles,and this could be avoided using enzymes from thermo-philes (Canganella and Wiegel 1993; Huber and Stetter1998; Bustard et al. 2000; Hong et al. 2009; Kumar et al.2009; Zhong et al. 2009). Research into thermophilicmicroorganisms has demonstrated that thermotolerant pro-teins are generally more stable than other proteins andretain this property when cloned and expressed in meso-philic bacteria (Connaris et al. 1998; Hayakawa et al.2009).

Psychrophiles

Definitions A psychrophilic prokaryote is defined by atemperature optimum for growth of 20 C, but able to grow well below 5 C,are designated as psychrotolerant. Bowman et al. (1997) usedthe term psychotroph; however, this wrong term (translatingto eating cold) is outdated and should not be used anymoredespite being used in older literature. Psychrophiles arelikely more abundant than one assumedsome aredifficult to culture. With no doubt, recent investigationinto naturally cold habitats has produced numerousculturable bacterial and archaeal species with temperatureoptima between 4 C and 15 C, as well as evidence formore novel taxa coming from genetic probes andmetabolic studies of non-cultured species living under

Fig. 3 Examples of model hotsprings in Uzon caldera, Kam-chatka, Russia

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these conditions. Some microorganisms are reported togrow at temperatures as low as 20 C. However, littlereproduced and confirmed data on pure cultures areavailable at this time; thus, the question about the lowestgrowth temperature has no answer yet.

Habitats Over 80% of the total biosphere of the Earth haspermanent temperatures of

Thomas 2000). However, with the development of propertechniques of cultivation, prokaryotes growing at up to113 C (Pyrolobus fumarii)and above under elevatedhydrostatic pressurehave been characterized from blacksmoker chimneys in deep ocean thermal vent environ-ments (Stetter 1996). This author divided the organismsinto hyperthermophiles (Topt > or =80 C), extremethermophiles (Topt 70 C to 80 C), and moderatethermophiles (Topt 45 C to 70 C), these being thegenerally adapted definitions (Mesbah and Wiegel 2008;Wagner and Wiegel 2008). Other classifications havebeen proposed in the past (e.g., Wiegel and Ljungdahl1996; Wiegel 1992), but should not be used anymore.One exception is the use of the term temperature-tolerant(extreme/hyper) thermophiles for thermophiles growingover an extended growth span of more than 35 C (Wiegel1990).

Habitats The naturally hot environments on Earth rangefrom terrestrial volcanic sites (including solfatara fields)with temperatures slightly above ambient to submarinehydrothermal systems (sediments, submarine volcanoes,fumaroles, and vents) with temperatures exceeding 300 C,subterranean sites such as oil reserves, and solar-heatedsurface soils with temperatures up to 65 C. There are alsohuman-made hot environments such as compost piles(usually around 6070 C but as high as 100 C), slagheaps, industrial processes, and water heaters (Oshima andMoriya 2008). The deep sea is in general cold, but it is nowknown that there are areas of superheated water andwidespread still-hot volcanic ocean crust beneath the flanksof the mid-ocean ridge and other rock structures, as well asgeothermally heated shallower ocean waters. Many envi-ronments are temporarily hot, adaptation to which may bethe reason that some thermophiles are very fast growing.Among the geothermally heated habitats are the alkaline,mainly carbonate-containing hot springs around neutral pHand acidic areas including some mud holes. Most of theacidic high-temperature habitats contain elemental sulfurand metal sulfides, and most isolates from these areasmetabolize sulfur by either anaerobic respiration or fermen-tation. Ocean depths are under extreme pressures from theweight of the water column, and thus, most isolates fromthese areas are piezotolerant, some are truly piezophilic,others such as Pyrococcus strain ES4 and Methanococcuskandleri show extensions of Tmax under increased pressure(Pledger et al. 1994; Summit et al. 1998, Takai et al. 2008),and all are at least halotolerant (Adams 1999), while thoseisolated from solfataras are generally acidophilic. Whilemost described species of obligately aerobic thermophilicarchaea are acidophilic, the anaerobic thermophilic bacteriaare generally unable to grow at acidic pH, but manyanaerobic bacteria and some archaea grow at alkaline pH

(Wiegel 1998). The anaerobic alkali thermophilic bacteriathus form an interesting group to study and their relation-ships between temperature optimum and pH optimum forgrowth are presented in Fig. 4. This adaptability to high pHenvironments involves both cellular and biomolecularpeculiar traits that are currently under investigation,particularly to exploit their potential applications.

Hyperthermophiles

Most of the hyperthermophilic organisms are archaea, andmany of these perform common metabolic processes suchas methanogenesis; anaerobic respiration via sulfate reduc-tion, sulfur reduction, nitrate reduction, iron reduction, etc.;aerobic respiration; or even fermentation. P. fumarii had fora long time the highest Tmax (113 C), a Topt of 106 C,being unable to grow below 90 C. However, the record isheld by M. kandleri strain isolated from the deep ocean nearJapan with a Tmax of 122 C under high atmosphericpressure (Takai et al. 2008). The discovery of deep-seahydrothermal vents in 1977 opened the way for the firststudy of an ecosystem based on primary production ofchemosynthetic extreme and hyperthermophilic bacteria(Prieur et al. 1995). Representative genera includeArchaeoglobus, Thermodiscus, Thermoproteus, Acidianus,Pyrococcus, Thermococcus, and Desulfurococcus, whichreduce sulfur or sulfate; Sulfolobus, which can oxidizeH2S or elemental sulfur; the methanogens Methanother-mus, Methanococcus, and Methanopyrus; and the nitratereducers Pyrobaculum and Pyrolobus. Sulfolobus andAcidianus isolates can also oxidize ferrous iron and withno doubt such a process plays a major role in the localenvironment and biogeochemical cycles. Examples ofhyperthermophilic bacteria are included in the generaThermotoga and Aquifex.

A great novelty was represented by the first descriptionof Nanoarchaea (Vainshtein and Kudryashova 2000;Branciamore et al. 2008; Podar et al. 2008; Burghardt etal. 2009) and these microorganisms have drawn theattention of deep-sea hydrothermal vent investigators. Awork describing the colonization of nascent, deep-seahydrothermal vents by novel archaeal and nanoarchaealassemblages was reported by McCliment et al. (2006).

Extreme and moderate thermophiles

Extreme thermophiles as bacteria include the anaerobicFirmicutes, the cellulolytic Caldicellulosiruptor saccharo-lyticus (Rainey et al. 1994), the ethanol-producing Ther-moanaerobacterium ethanolicus (Wiegel 1992; Wiegel andLjungdahl 1996), as well as the acetogenic facultativechemolithoautotrophic Thermoanaerobacterium kivui


(Leigh and Wolfe 1983) and Ammonifex degensii, the latterbeing capable of forming ammonium from nitrate viachemolithoautotrophic growth (Huber et al. 1996). Amongthe aerobic ones are the well-known Bacillus stearother-mophilus (Firmicutes) and some species within the Gram-type negative genus Thermus which can be isolated fromhot water boilers. Recently novel thermophilic species weredescribed, interesting for both basic and applied scientificissues: the citrate-fermenting Sporolituus thermophilus(Ogg and Patel 2009), the novel bacterial phylumCaldiseria (Mori et al. 2009), the deep-sea bacteriumNautilia abyssi (Alain et al. 2009), the thermal mud-inhabiting Anoxibacillus thermarum (Poli et al. 2009), andthe novel microaerophilic, nitrate- and nitrite-reducingthermophilic bacterium Microaerobacter geothermalis(Khelifi et al. 2010).

Among the moderate thermophiles and thermotolerantorganisms are the cellulolytic Clostridium thermocellum,the acetogenic Moorella thermoacetica/thermoautotrophica,and Thermoanaerobacterium (former Clostridium) thermo-saccharolyticum, capable of growing in vacuum-packedfoods and thus known as the can-swelling organism(Kristjansson 1992; Wiegel and Canganella 2000; Prevostet al. 2010). The obligate mixotrophic Thiomonas bhuba-neswarensis, the marine Lutaonella thermophila, the cellu-lolytic bacteria Clostridium clariflavum and Clostridiumcaenicola, the facultative microaerophilic Caldinitratiruptormicroaerophilus, and a novel hydrogen-producing bacteriumfrom buffalo dung were described (Arun et al. 2009; Pandaet al. 2009; Shiratori et al. 2009; Fardeau et al. 2010;Romano et al. 2010). The last overview on anaerobicthermophiles and their main properties was published byWagner and Wiegel (2008).

Evolutionary interest The hyperthermophilic organisms arecontained in the deepest, least evolved branches of the

universal phylogenetic tree (Fig. 5), often use substrateswhich are thought to have been predominant in theprimordial terrestrial makeup, and produce substanceswhich predominate in the present geochemistryindicationsthat they could have been the first life forms on thisplanet (Wiegel and Adams 1998). This is possible and itis one reason why thermophiles are studied so extensively.The study into how they manage thermostability at theprotein and membrane structural level has elucidated manytraits of the protein, membrane, and nucleic acid structure;however, there is not yet a full understanding of theprinciples of thermostability (Daniel 1996; Vieille andZeikus 2001; Basu and Sen 2009; Kim et al. 2009;Averhoff and Mller 2010). The development of bettergenetic tools for use with these organisms portends formore practical applications in the future (Bustard et al.2000).

Extremes of pH

The cells of humans and of other higher life forms existstably only within a narrow pH range, with a value around7.4 often referred to as physiologic. Marine fish andinvertebrates do best with an external pH range of 8.18.4,the pH of ocean water.

One might expect that microorganisms would requirethat the pH of the external medium conforms to an equallynarrow or even narrower range of acidity or alkalinity, butthis is not generally the case. Microorganisms are able tothrive in a wider range of pH than most human and othereukaryotic cells do, and some even require extremes oneither the acidic or alkaline ends of the scale, without theability to survive exposure to neutral pH. Obviously, manybacteria have been known for years to live in moderately

Fig. 4 Relationship betweentemperature optima and pHoptima for growth of represen-tative anaerobic thermophilicbacteria. Note that the mostacidic pHopt is only in theacidotolerant range, while thereare several alkaliphiles (fromWiegel 1998)


low pH, such as those which are used in food fermentationsand do well at pH as low as 4.5 (Stiles and Holzapfel 1997;Caplice and Fitzgerald 1999). However, in the past, it hasbeen assumed that nothing could live at pH 0 or abovepH 11, but now many species of bacteria and archaea areknown which not only can live at these extremes but alsorequire them (e.g., Picrophilus species can grow at pH 0 at60 C) as a result of evolutionary processes (Poli et al.2007; Hou et al. 2008; Zhou et al. 2008; Johnson et al.2009).

Research and development has been particularlyfocusing on the potential use of mesophilic and psychro-philic acidophiles for biomining such as tank leachingprocesses and heap leaching processes. Moreover, theapplication of moderately thermophilic and extremelythermophilic acidophiles for biomining and in thetreatment of both refractory gold-bearing and basemetalmineral sulfide concentrates has also been extensivelyinvestigated (Johnson 1995; Das et al. 1999; Castro and

Moore 2000; Johnson 2001; Dopson et al. 2004; Rawlingsand Johnson 2007; Johnson and Hallberg 2008; Cardenaset al. 2010; Dopson 2011). Some research activitiesregarded the problems of arsenic toxicity to certain strainsof moderately thermophilic bacteria when oxidizing bothrefractory gold and basemetal sulfide concentrates. Otherpotential applications of thermophilic acidophiles areusually related to the mineral industry and in allieddisciplines including treatment of metalliferous minewastes, acid mine waters, and sulfurous gases.

Though earlier reports occurred on the isolation ofalkaliphilic organisms from human and animal feces(Vedder 1934), the first systematic study of alkaliphilicprokaryotes was undertaken in the early 1970s, specificallyto look for industrially useful enzymes (Horikoshi 1971).Indeed, alkaliphilic bacteria (able to grow above pH 10,with a pHopt around 9, and unable to grow at pH 7 or lessKumar and Takagi 1999) were used anonymously forcenturies in processing dye from indigo plants, though

Fig. 5 Phylogenetic tree high-lighting possible evolutionaryrelatedness of hyperthermo-philes. From Huber and Stetter(1998), after Woese et al. (1990)


only cultured and isolated in the last century (Takahara andTanabe 1960). This group of extremophiles is anotherexample of potential usefulness, with alkaline proteases andcellulases adapted for use in laundry and other detergents(Horikoshi 1996), xylanases for use in the pulp/paperindustry (Nakamura et al. 1993), and lipases in bioprocessingof lipids (Bornscheuer et al. 2002; Salameh and Wiegel2007). Enzymes of alkaliphiles are also used for dehairing ofhides in leather tanning, making of food additives, and drugmanufacture. One particularly important industrial applica-tion has been the production of cyclodextrin for use infoodstuffs, chemicals, and pharmaceuticals, using alkalinecyclomaltodextrin glucanotransferase (Horikoshi 1996);moreover, other possible applications are being exploredfor enzymes from these organisms (Asha Poorna and Prema2007; Singh et al. 2008).

Acidophiles

Definitions It is generally accepted to define acidophilicorganisms as those which can grow at pH values lower than5 and showing pH optima between 2 and 4. The fact thatmicroorganisms growing at pH values close to 0 have beendescribed will certainly expand further the group of theso-called extremely acidophilic organisms.

Most acidophiles have evolved extremely efficient mech-anisms to keep the cytoplasm at or near neutral pH, andseveral processes are associated with pH homeostasis inacidophiles (Johnson 1998; Booth 1985; Dopson et al. 2004;Baker-Austin and Dopson 2007): (1) Acidophiles reverse thereversed membrane potential to partially deflect the inwardflow of protons. One potential mechanism of generating areversed membrane potential is by potassium transportapredominance of potassium-transporting ATPases is found inacidophile genomes. (2) Many acidophiles have evolvedhighly impermeable cell membranes to retard the influx ofprotons into the cell. (3) pH is maintained through activeproton export by transporters. (4) The sequencing of severalacidophile genome sequences has indicated that there is ahigher proportion of secondary transporters than in neutra-lophiles. Overall, they reduce the energy demands associatedwith pumping necessary solutes and nutrients into the cell.(5) The presence and availability of enzymes and/orchemicals capable of binding and sequestering protons mighthelp maintain pH homeostasis. (6) Comparative genomeanalysis suggests that a larger proportion of DNA andprotein repair systems might be present in acidophilescompared with neutralophiles and that this could beassociated with the cellular demands of life at low pH. (7)Organic acids that function as uncouplers in acidophilesmight be degraded by heterotrophic acidophiles.

Studies of proteins adapted to low pH have revealed a fewgeneral mechanisms by which, for instance, proteins can

achieve acid stability. In most acid-stable proteins (such aspepsin and the soxF protein from Sulfolobus acidocaldarius),there is an overabundance of acidic residues which minimizeslow pH destabilization induced by a buildup of positivecharge. Other mechanisms include minimization of solventaccessibility of acidic residues or binding of metal cofactors.

As far as life at high temperature is concerned, somemicroorganisms tend to use a higher proportion of purinesin their codons, which are more resistant to heat denaturationthan pyrimidines, but unfortunately, at low pH, purines arehighly susceptible to acid hydrolysis. Some thermophilicacidophiles have adapted to growth at high temperatures by ageneral increase in the concentration of purine-containingcodons as a heat-stabilizing adaptation, while simultaneouslyreducing the concentration of purine-containing codons inlong open reading frames that are more prone to acidhydrolysis-associated mutations.

Habitats and biochemistry Acidic habitats are abundant andthere are a number of natural processes which result in netacidity. Representatives among these may be several types ofprokaryotic metabolism, including nitrification, accumulationof organic acids during fermentative or aerobic metabolism,and the oxidation of elemental sulfur, reduced sulfurcompounds (RSCs) and ferrous iron (especially in the formof pyrite). Some soils of volcanic origin, such as in solfatarasand fumaroles, are generally acidic and rich in elementalsulfur or sulfidic ores, as are many hot springs and areas whichsurround them. However, the majority of extremely acidichabitats are at least partially anthropogenic, owing theirexistence to one particular human activitythe mining ofmetals and coal (Johnson 1998; Bond et al. 2000). Thesehabitats include coal refuse piles; abandoned mine shafts orpits; copper-leaching dumps; and soils, rivers, or lakescontaminated by acidic runoff from these sites. There is asynergy at work, in that many valuable metals (i.e., likely tobe mined) occur as sulfide ores, and acidophilic micro-organisms are often able to oxidize the sulfides such that netacidity in the form of sulfuric acid results. The dissimilatoryoxidation of metal sulfides (where Me represents a cationicmetal) can be written as: Me2+S2 (insoluble metal complex)Me2++SO4

2. When water is available, sulfuric acid willform and cationic metals and metalloid elements (iron, zinc,copper, aluminum, lead, and arsenic) will be solubilized: theprocess is referred to as microbial ore leaching (Johnson2001). The biological activities of ore leaching require airand water in addition to the metal sulfide substratesasituation available in coal spoils, pit lakes, abandoned mines,and other such sites exposed to air and rainwater. Contam-ination of lakes, rivers, soils, and groundwater by acid minedrainage and runoff not only acidifies these sites but alsobrings the solubilized metals to often toxic levels. Muchindustrial interest has been shown on extreme acidophiles,


with subsequent application having been successful in thearea of biomining: the use of acidic bioprocesses to removevaluable metallic minerals from sulfide ores (Das et al.1999). Other uses are envisioned: acidophilic sulfatereducers may actually contribute net alkalinity to the sitesand could be used for acid mine drainage remediation(Johnson 1995; Castro and Moore 2000); the utilization ofaliphatic compounds by some acidophiles, in combinationwith their tolerance of heavy metals, makes them candidatesfor bioremediation of acidic wastewaters contaminated withtoxic organic compounds and heavy metals (Gemmell andKnowles 2000). Most of the prokaryotes useful in theseareas are extreme acidophiles, with pHopt

Eukaryotic heterotrophs which inhabit extremely acidicsites include species of the yeasts Rhodotorula, Candida, andCryptococcus. The filamentous fungi Acontium cylatium,Trichosporon cerebriae, and a Cephalosporium sp. can growaround pH 0 (Schleper et al. 1995). Protozoa have also beenisolated which are obligately acidophilic, such as Eutreptial/Bodo spp., Cinetochilium sp., and Vahlkampfia sp., whichcan grow as low as pH 1.6 and graze mineral-oxidizing andother acidophilic bacteria (Johnson and Rang 1993).

Alkaliphiles

Definitions As with most extremophilic categories, thereare many subdivisions to be made, but a simplistic division

implies to define alkalitolerant organisms as those whichcan grow at a pH of 9 or 10 but which have pH optima nearneutrality (Krulwich 1986; Krulwich and Guffanati 1989;Wiegel 1998). On the other hand, the term alkaliphile isused for microorganisms that grow optimally or very wellat pH values above 9 but cannot grow or grow only slowlyat the near neutral pH value of 6.5. Many different taxa arerepresented among the alkaliphiles, and some of these havebeen proposed as new taxa. Alkaliphiles can be isolatedfrom normal environments such as garden soil, althoughviable counts of alkaliphiles are higher in samples fromalkaline environments. The cell surface may play a key role inkeeping the intracellular pH value in the range between 7 and8.5, allowing alkaliphiles to thrive in alkaline environments,although adaptation mechanisms have not yet been clarified.

Table 2 Representative acidophilic prokaryotes grouped by growth temperature optima, with relevant metabolic features noted

Temperature designation Metabolic feature Examples

Mesophilic Autotrophic iron and sulfur oxidation Acidithiobacillus ferrooxidans

Thiobacillus prosperus

Autotrophic, only oxidizes iron Leptospirillum ferrooxidans

Autotrophic oxidation of RSCs but not iron Acidithiobacillus thiooxidans

Acidithiobacillus albertensis

Heterotrophic Ferromicrobium acidophilusIron oxidation

Heterotrophic or mixotrophic sulfur oxidation Acidithiobacillus acidophilus

Thiomonas cuprinus

Sulfobacillus disulfidooxidans

Obligately organoheterotrophic Acidiphilium

Acidocella

Acidomonas methanolica

Acidobacterium capsulatum

Moderately thermophilic Iron oxidation Leptospirillum thermoferrooxidans

Oxidation of RSCs but not iron Acidithiobacillus caldus

Heterotrophic or autotrophic iron oxidation Sulfobacillus acidophilus

Sulfobacillus thermosulfidooxidans

Acidimicrobium ferrooxidans

Obligately organoheterotrophic Alicyclobacillus

Thermoplasma acidophilus

Thermoplasma volcanium

Picrophilus oshimae

Picrophilus torridus

Extremely thermophilic Iron oxidation Acidianus (several species)

Sulfurococcus yellowstonii

Metallosphaera sedula

Oxidation of RSCs and iron Sulfolobus metallicus

Heterotrophic or mixotrophic sulfur oxidation Sulfolobus shibatae

Sulfolobus solfataricus

Sulfolobus hakonensis

Sulfurococcus mirabilis

Metallosphaera prunae


Habitats Naturally extremely alkaline environments occurin soda lakes, where high evaporation rates in closeddrainage basins occur. The water contains scarce amountsof Mg2+ and Ca2+ and is near-saturated with sodium salts,especially chloride, carbonate, and bicarbonate, with the pHgenerally around 10 due to high levels of sodium carbonate(Duckworth et al. 1996). Alkaline environments also arenoted in pockets in ordinary soils where transient alkalinityis proposed due to various biological activities (Grant et al.1990)indeed, alkaliphilic microorganisms have oftenbeen isolated from ordinary soils and other non-alkalineenvironments (Jones et al. 1998; Wiegel 1998). A fewnatural habitats are hypersaline and alkaline, harboring alarge group of haloalkaliphiles, especially from LakeMagadi, Kenya, the Wadi Natrun Lakes in Egypt (Imhoffet al. 1978, Mesbah et al. 2009), and recently from sodalakes of Kulunda Steppe in Altai, Russia (Sorokin andMuyzer 2010a, b). Many of these organisms are alsothermotolerant to various degrees, making these lakesinteresting sources of novel microorganisms (Jones et al.1998; McGenity et al. 2000). Man-made alkaline environ-ments include effluents from tanneries, paper mills, foodand textile processing plants, calcium carbonate kilns,detergents, and other industrial processes. They all have incommon high levels of sodium [though it may be as low as5% (w/v)] and concentrations of carbonate and bicarbonatewhich greatly exceed those of Mg2+ and Ca2+. Thus, theMg2+ and Ca2+ tend to precipitate as insoluble compoundswith carbonate, leaving the excess anion to form sodiumsalts and counter the buffering effect of CO2. In addition,microbial processes such as ammonification and sulfatereduction lend to the establishment of a stable, perpetuallyalkaline environment (Cavicchioli and Thomas 2000).

Organisms Taxonomic groupings of alkaliphilic prokar-yotes include, within the cyanobacteria, some members ofthe order Chroococcales and several species within thegenus Spirulina. Alkaliphiles within the aerobic Firmicutesare widespread and include members of the order Actino-mycetales, the families Micrococcacceae, the genera Strep-tomyces, and Nocardia and related actinomycetes andvarious genera within the order Bacillales (see BergeysManual for new Systematic). Among the anaerobic alka-liphiles are various members of families within the ordersClostridiales, Haloanaerobiales, and Natranaerobiales.The Proteobacteria contain many alkaliphiles, especiallythe gamma subdivisions Ectothiorhodospira, Halomona-daceae, and Pseudomonas. Moreover, an alkaliphilic andhalophilic member of the Thermotogales was isolated,Thermopallium natronophilum (Duckworth et al 1996).The Archaea contain many alkaliphiles, namely within theEuryarchaeota: Halorubrum vacuolatum, Natrialba maga-dii, several Natronobacterium species, and several Natro-

nococcus species. Alkaliphilic Methanomicrobiales includeseveral species of Methanohalophilus.

Ecology and physiology Alkaliphiles have important rolesin their native ecosystems. High primary productivities areseen in soda lakes in East Africa, as a result of densepopulations of cyanobacteria provided with nearly unlimitedsupplies of CO2, high ambient temperatures, and high dailylight intensities. This presumably supports the heterotrophicmembers of the microbial community, and a diversity ofmicrobial metabolism, such as hydrogenotrophic sulfatereduction, acetogenesis, sulfur oxidation, and methaneoxidation is also seen (Duckworth et al. 1996). Somealkaliphiles are anaerobic, many are halophilic, and mostare halotolerant (Zhilina et al. 1996), and while most grow inthe mesophilic temperature range, there are also someinteresting (halophilic) alkalithermophiles (Wiegel 1998;Mesbah and Wiegel 2008).

As with halophiles, discussed in the next section, alka-liphiles require sodium ions for normal growth and metabo-lism. One would expect a number of unique adaptations to lifewithin an ambient pH of 10 or greater. It was noted early thatintracellular enzymes from these organisms had highest ratesof catalysis at near neutral pH, while for excreted enzymes,the highest catalytic rates were noted at nearer the optimumgrowth pH for the organism (Larson and Kallio 1954). Thisobservation led investigators to assume that intracellular pHwas somehow kept near neutrality in these organisms.Indeed, this has been confirmed by further observations(Padan et al. 2005), showing aerobic alkaliphiles generallymaintain their cytoplasmic pH about 2 units lower thanambient pH, anaerobes around 1 pH unit (Mesbah et al.2009). Sodium ions are necessary for keeping intracellularH+ relatively high (despite, at least in aerobes, respiratoryactivity which extrudes protonsKrulwich et al. 1996;Krulwich and Guffanati 1989), with active extrusion ofsodium ions coupled to importation of protons against bothgradients by Na+/H+ antiporters (Buck and Smith 1995).Many membranes in alkaliphiles are reported to containsodium-coupled ATPases (similar to those of halophiles) aswell as, or rather than, proton-coupled ATPases (Kaieda etal. 1998; Koyama 1999; Ueno et al. 2000); however, otherdata go against this (Cavicchioli and Thomas 2000). Manyof these systems are similar to those of halophiles, even inalkaliphiles which are not strictly halophilic, but are at leasthalotolerant.

Extremes of salinity

Higher organisms can be divided between those whose cellsrequire relatively low (i.e., 0% to 0.9% for humans


normal or physiological) NaCl concentrations andthose whose cells require elevated concentrations (i.e.,marine fish do best at 3% NaClthe salinity of oceanwater and human tears). However, the very high saltconcentrations in hypersaline lakes or soils, salterns, orother man-made environments such as salted foodspreclude the growth of most fish, invertebrate animals,plants, and even most prokaryotesbut there are micro-organisms which thrive there. Marine microorganisms,like marine fish, mammals, and invertebrates, must at leasttolerate ocean water salinity. In contrast to halotolerantorganisms, obligate halophiles must require NaCl concen-trations higher than 3% (wt/vol) for optimal growth. Therequirement for NaCl may be slight [most rapid growth at2% to 5% (0.34 to 0.85 M) NaCl], moderate [most rapidgrowth at 5% to 20% (0.85 to 3.4 M) NaCl], or extreme[most rapid growth at 20% to 30% (3.4 to 5.1 M) NaCl](Larsen 1962). Other definitions have been publishedincluding that true halophiles grow optimally at and above10% NaCl.

Basic research into halophilicity of proteins andmembranes, osmoregulation, and genetics of these organisms,especially of archaea, is voluminous. Several practicalapplications are envisioned from the study of halophiles:better understanding of salted, fermented foods technology;remediation of saline wastewater (Kargi and Dincer 1998;Kargi and Dincer 2000); and bioremediation of toxiccompounds such as uranium (Francis et al. 2000),hydrocarbons (Bruns and Berthe-Corti 2000; McGenity2010), and pollutants (Le Borgne et al. 2008). Further-more, the production of biopolymer has been describedfor bacterial and archaeal halophilic microorganisms(Hezayen et al. 2000; Mata et al. 2008 ; Van-Thuoc et al.2008; Quillaguamn et al. 2009).

The halophiles

Definitions The most accepted definitions presently usedare those from Oren (2006). Many organisms are referred toas halotolerant or slightly halotolerant, which generallymean that the organism grows best with 00.5% NaClconcentrations but can tolerate various higher concentra-tions such as up to 3% NaCl which normally is encounteredin marine environments. The salt requirement and toleranceparameters are highly dependent on temperature, pH, andgrowth medium: a halotolerant organism grown in complexmedia (such as Halomonas elongateVreeland et al. 1980)was found to be truly halophilic when grown in minimalmedia under otherwise identical conditions (Canovas et al.1996). An interesting phenomenon was found recentlytherequirement of chloride ions for (moderate) halophiles(Roeler and Mller 2002; Bowers and Wiegel, unpub-lished results).

Habitats The habitats which contain high salt concentra-tions are diverse. Some authors feel that understanding ofthe adaptations of terrestrial halophilic archaea may beimportant in the detection of life on Mars, assuming similartypes of salts and a carbon-based life form (Litchfield1998). Several of the hypersaline soda lakes (LakeMagadi in Kenya; the Wadi Natrun lakes in Egypt; andMono Lake, Big Soda Lake, and Soap Lake in the WesternUSA) are highly alkaline, with pH values of 9 to 11, whilethe Great Salt Lake and the Dead Sea have pHs around 7(Ollivier et al. 1994). Unusual habitats have been found tobe populated with halophiles, such as the oil-field water inthe North Sea (Lien et al. 1998), preserved salted foods(Kobayashi et al. 2000), and the nasal cavities of desertiguanas (Deutch 1994; Lawson et al. 1996), though theocean, hypersaline lakes of oceanic (thalassohaline) or non-oceanic (athalassohaline) origin and solar salterns make upthe predominant habitats (Antunes et al. 2008). Halotolerantor halophilic microorganisms have also been isolated frompolar sea ice (Bowman et al. 1998) and from Antarcticrocks (Smith et al. 2000). Salinities in the various habitatscan range from that of brackish waters to saturation, orfrom about 0.5% to 37% or more. The predominant saltsare often Na+ and/or Cl, though Mg++ or Ca++ may be inabundance (except in the soda lakes, see section onAlkaliphiles), and all are usually noted in higher concen-trations than in more moderate habitats. Sulfate is generallyan important electron acceptor in these ecosystems, andsalterns generally show precipitation of calcium compounds(CaSO4 and CaCO3) as well as NaCl, while soda lakes havecarbonate precipitates of magnesium and calcium, withlittle of these cations in solution.

Physiology Halophilic prokaryotes generally require sodi-um ions for optimal growth, as they are coupled to activeuptake of nutrients, the working of the membrane respira-tory chain, and making of ATP (Unemoto 2000). Con-versely, and often intimately linked, is the need to controlthe net diffusion of sodium ions into the cytoplasm from thehypersaline environment to avoid toxic cytoplasmic sodiumlevels. Many halophilic bacteria maintain elevated levels ofsodium ion in their cytoplasms, with their intracellularstructures and enzymes adapted to and dependent on thoselevels; they may employ energy-consuming processes toactively extrude excess sodium (Deppenmeier et al. 1999;Eddy and Jablonski 2000). The gradient of sodium ionsthus maintained across cell membranes can be utilized bythe organisms. For example, in some methanogens (halo-philic or not), a reversible sodium ion pump is utilized,coupling the process of methyl transfer to the transport ofNa+ across the cytoplasmic membrane. Other ion pumpsgenerate proton motive force by redox-potential-drivenproton translocation. Thus, both a sodium ion gradient


and an electrochemical proton gradient are generated bythe organisms, with both ion gradients used directly inthe synthesis of ATP, in the case of Na+ by a sodium-dependent ATP synthase (Deppenmeier et al. 1996;Baumer et al. 2000). Several acetogens use a similarprocess to couple acetogenesis with ATP production(Heise et al. 1992). Marine and other halophilic bacteriahave a sodium pump as an integral part of their electrontransport chain (the NADH-quinone reductase) whicheffectively couples ATP production with extrusion ofsodium ions from the cell. A similar sodium ion pump isfound in many non-halophilic, Gram-type negative path-ogenic bacteria, adding new insights into their physiologyas well (Unemoto and Hayashi 1993). Many halotolerantor halophilic organisms, including the halotolerant micro-alga Dunaliella maritima (Shumkova et al. 2000), couplethe extrusion of sodium ions to the importation ofsubstances such as amino acids, utilizing ATP in theprocess (Unemoto 2000). Thus, the adaptations of copingwith elevated sodium and the requirement for elevatedsodium are intricately linked.

Prokaryotes living in hypersaline environments mustequalize the osmolarity within and without their cellularenvelopes in order to remain intact. Some do this bymaintaining high intracellular ionic strength (with KCl orNaCl levelsGalinski and Trper 1994; Danson andHough 1997) or by accumulating organic solutes (Roberts2005; Empadinhas and da Costa 2008 and literature citedtherein).

In these organisms, complex intracellular adjustmentsand unique properties of the cytoplasmic membranes allowexistence in the high ionic strength environment. Theirenzymatic and structural proteins are also adapted tofunction in the high-solute load environment; for example,intracellular enzymes from the obligately halophilic archaeaare often active and stable at multimolar salt concentrationsand denature below 2 to 3 M KCl (Eisenberg 1995). Aswith the hyperthermophiles, the most halophilic organismsare generally archaea, though a number of halophilicbacteria have also been isolated, even in environments withsodium chloride concentrations close to saturation (Antonet al. 2000; Bowers et al. 2009).

Organisms Halophilic prokaryotes include archaea andbacteria and both anaerobes and aerobes (Kamekura et al.1997; Kamekura 1998; Oren 2006; Ma et al. 2010).

The anaerobes bacterial halophiles are represented byfermentative, sulfate-reducing, and phototrophic genera andinclude psychrophiles, mesophiles, and thermophiles(Ollivier et al. 1994). Some of the orders contain onlyhalophiles such as the orders Natranaerobiales (type genusNatranaerobius; Mesbah et al. 2009) comprising only onefamily and two genera with halo-alkalithermophilic species

and the order Haloanaerobiales containing the two fami-lies: Haloanaerobiaceae (type genus Halanaerobium) andHalobacteroidaceae (type genus: Halobacteroides) [for anupdated list see the website http://www.bacterio.cict.fr/classifgenerafamilies.htm]. For example, the species ofHaloanaerobium, Haloanaerobacter, and Haloincola livein ranges from 2% to 30% NaCl, with optima from 10% to18%, and the species of Halobacteroides grow in a NaClrange of 5% to 30% with optima from 9% to 18%. Table 3summarizes some of the characteristics for representativeanaerobic and fermentative halophilic bacteria.

The slightly to moderately halophilic sulfate-reducingbacteria (SRBs) are found within various genera: Desulfo-vibrio, Desulfobacter, Desulfotomaculum, Desulfococcus,Desulfobacterium, Desulfonema, and Desulfohalobium. Allcan be defined as slight halophiles except for Desulfovibriohalophilus and Desulfohalobium retbaense, which aremoderate halophiles. The latter has a salinity range of 3%to 25% NaCl with an optimum of 10% NaCl. Theanoxygenic phototrophic halophiles include Chromatium,Chlorobium, Rhodospirillum, Rhodobacter, Thiocapsa, andEctothiorhodospira, as well as others and span the gamut ofNaCl requirements. Two species, Halorhodospira halophilaand Halorhodospira halochloris, are extreme halophiles(Imhoff and Trper 1977).

Among the halophilic anaerobic archaea are the meth-anogenic genera Methanohalophilus, Methanosalsum, andMethanohalobium, which contain moderate and extremehalophiles, as well as the halotolerant genus Methanocal-culus (Ollivier et al. 1998), which tolerates salinities of 012% with an optimum for growth of 5% NaCl, and theslightly halophilic Methanogenium.

Halophilic aerobic bacteria (Ventosa et al. 1998b) includeall genera and species within the Gram-type negative familyHalomonadaceae, in the phylum of Proteobacteria (Arahaland Ventosa 2006; Arahal et al. 2007). The genus Glaciecolawas also described within the gamma subdivision of theProteobacteria, containing two aerobic, psychrophilic, slight-ly halophilic species (Bowman et al. 1998). The orderCytophagales, of the alpha subdivision of Proteobacteria,contains many halotolerant and halophilic genera. Thereare also several halophilic aerobic methylotrophic bacteria,such as Methylarcula marina (Doronina et al. 2000; Sorokinet al. 2007). Aerobic Gram-type positive halophiles belongexclusively to halophilic genera, such as Halobacillus,Marinococcus, Salinicoccus, Nesterenkonia, and Tetrageno-coccus. Several species belong to genera within the orderFirmicutes Salimicrobium halophilus, Gracilibacillus dipso-sauri (Lawson et al. 1996), Bacillus marismortui (Arahalet al. 1999), and Salibacillus salexigens (Garabito et al.1997). Several halophilic actinomycetes have been isolatedwhich belong to the genera Haloglycomyces, Saccharopoly-spora, Streptomonospora, Actinopolyspora, Nocardiopsis,


and Zhihengliuella (Ventosa et al 1998b; Cai et al. 2009;Tang et al. 2009; Guan et al. 2009; Chen et al. 2010).Ventosa et al. (1998a) reviewed excellently the diversity ofmoderately halophilic Gram-type positive bacteria.

In addition to the anaerobic archaea mentioned above arethe aerobic forms. These all lie within the familyHalobacteriaceae which has been authoritatively summa-rized by Oren et al. (1997) and include many novel generaall of which are strict halophiles.

Other halophilic extremophiles Unusual halophiles are theHaloplasma contractile (Haloplasmataceae) isolates, awall-less contractile bacterium isolated from the Red Sea,as well as the above mentioned members of the OrderNatranaerobiales. The later ones are polyextremophilic, i.e.,anaerobic halophilic alkalithermophilic bacteria isolated fromathalassohaline salt lakes in Egypt and the Kenyan Rift Valley,able to grow under the combined conditions of up tosaturation of NaCl in the presence of sodium carbonates, atpH values above 10 and temperatures as high as 70 C andthus thrive at the present boundaries of live for combinedstressors (Bowers et al. 2009).

Extremes of hydrostatic pressure

The piezophiles

Definitions The term obligate, or extreme, piezophile hasbeen used for an organism incapable of growth atatmospheric pressure regardless of temperature, while theterm piezotolerant has been applied to an organism which

grows best at atmospheric pressure but which can also grow atelevated pressures. One definition states also that extremelypiezophilic bacteria are those unable to grow at pressure

symbol of deep-sea vent animal communities for many years.These sulfur-oxidizing and carbon-fixing microorganisms arepresent in enormous numbers inside the animals body andthey are capable of supplying most of the worms metabolicneeds thanks to the fixation and incorporation of CO2(Cavanaugh et al. 1981; Robidart et al. 2008).

In most cases, the response to pressure is greatest nearthe organisms upper temperature limit for growth, or someorganisms may experience an elevated Tmax at higherpressures (Summit et al. 1998).

Psychrophilic obligate piezophiles generally belong toone of five genera of the gamma-proteobacteria: Photo-bacterium, Shewanella, Colwellia, Moritella, Psychromo-nas, and to a new group containing the strain CNPT3(Delong et al. 1997). Among hyperthermophilic piezo-philes, the archaeon Thermococcus barophilus (Marteinssonet al. 1999) and Pyrococcus species have been described(Zeng et al. 2009). The most striking example of elevatedpressure effects on a microorganism is the above mentionedM. kandleri, which under high pressure is able to growat 122 C. How pressure does affect in such a case theupper temperature limit for growth was only partiallyinvestigated; it seems that the soluble H2 concentrationin the liquid phase was the most significant parameter tocontrol the G of hydrogenotrophic methanogenesisunder different growth conditions and that the correlationmay be mainly explained by the kinetic effect of theelevated H2 concentration.

Much research has focused on the membrane lipidcomposition in response to elevated pressures, looking athow proper fluidity of the membrane is maintained (Yano etal. 1998; Fang et al. 2000). Genetic research has identifiedgenes in piezophiles and in bacteria adapted to live atatmospheric pressure as well, which are regulated bychanges in pressure (Kato et al. 1996b). Responses totemperature and pressure changes are similar in the twogroups of organismsimplying that the mechanisms arewidely conserved and that in general bacterial growth ratesmay be stimulated by high pressure near their maximumtemperature for growth.

A number of piezophiles have been found to be tolerantto high concentrations of organic solvents, as well as thosewhich are merely tolerant to both conditions. Similar tothermophiles, the cardinal temperatures of psychrophilescan differ when they are grown at various pressures(Patching and Eardly 1997; Bakermans et al. 2009).

Radiation resistance

Electromagnetic radiation of various types continuouslybombards the biosphere of the Earth, some being natural

and some owing its origin to human activities. At a shorterwavelength, higher energy radiation such as gamma raysand X-rays, are referred to as ionizing radiation becausethey can cause atoms to lose electrons or ionize. Thebombardment of DNA by X-rays frequently damages thebases or causes breaks in the backbone, inducing mutationsor even causing death of the organism. Ultravioletradiation, next and longer in wavelength to X-rays,primarily does damage to DNA by formation of thyminedimers. Most organisms have mechanisms with which torepair this damage, with varying success. Fortunately, mostUV radiation is absorbed by the Earths atmosphere,including the ozone layer, prior to reaching the surface.Visible light and higher wavelength infrared and radio-waves are less damaging to cellular structures. Areas of theEarth where the atmosphere is thin (some areas near thePoles, especially with the seasonal increase and decrease inthe ozone hole) and those exposed to high amounts ofsunlight (near the Equator) receive more radiation thanothers. Microorganisms can in general resist ionizing andother forms of radiation, or at least cope with their damageand resultant mutations, better than can higher organisms,possibly owing to their single-celled organismal structure.Certain pigments (i.e., carotenoids, melanin) are used byvarious organisms to absorb or quench the damaging effectsof various forms of radiation.

Certain microorganisms have developed highly adaptedsystems for dealing with radiation. Many Firmicutes areable to form endospores, which in addition to protecting theDNA from damage by placing it in association with small,acid-soluble spore proteins, also have particular DNAreactions to radiation (i.e., spore photoproduct) as well asparticular repair mechanisms active at germination (Setlow1994; Fajardo-Cavazos and Nicholson 2000). The familyDeinococcaceae containing the genus Deinococcus isradioresistant as vegetative cells, even to large doses ofionizing radiation (Zhang et al. 2007; Shashidhar andBandekar 2009; Yuan et al. 2009). They contain highlyactive DNA repair systems and several copies of theirgenomes to use as templates for replacing and repairingradiation-damaged DNA (Battista 1997). Furthermore, ithas been demonstrated that specific proteins are extremelyimportant in the gamma radiation resistance of Deinococcusradiodurans and related taxa (Hua et al. 2010; Shuryak andBrenner 2010). Many novel Deinococcus species wererecently isolated from areas such as the Atacama Desert dueto the direct correlation and similar mechanisms for dryresistance and gamma radiation resistance. While Deinococ-cus species do not require radiation to live, this extremeresistance qualifies them to be mentioned in this mini-review. Kineococcus radiodurans is another highlyradiation-resistant bacteria (Phillips et al. 2002). As men-tioned in the previous section, the ultramicrobacterium


Sphingomonas is also quite resistant to UV-B radiation. Thedesiccation-resistant cyanobacterium Chroococcidiopsis,which usually lives in deserts and hypersaline environments,is also quite resistant to ionizing radiation (Billi et al. 2000).Other genera or species of prokaryotes have shown to exhibitelevated resistance to gamma and UV radiation such asHymenobacter xinjiangensis (Zhang et al. 2007), butsignificant resistance (i.e. at the level of Deinococcus) hasrarely been reported.

Desiccation resistance

The capability to tolerate extreme desiccation conditionshas been investigated in the last decades, particularly as faras exobiology is concerned, so further data and referencesare reported in that specific chapter.

Some of the research activities were focused on thetaxonomy and metabolism of psychrophilic bacteria andyeasts, but desiccation tolerance properties have especiallybeen described in lichens. More specific insights into thephysiology and molecular traits of microorganisms capable towithstand extreme desiccation conditions were obtained look-ing at exopolysaccharide composition and production inphototrophic isolates (Knowles and Castenholz 2008; Ozturkand Aslim 2009), cell structure and metabolism in lichens(Aubert et al. 2007; Jonsson et al. 2008; Heber et al. 2009),survival and stress response (Stevens 1997; Khmelenina et al.1999; Beblo et al. 2009; Gorbushina and Broughton 2009;Ozturk and Aslim 2009; Smith et al. 2009), and genetictransfer (Billi et al. 2001). Other researches focused on themicroorganisms living inside 13 in. of translucent rocksincluding the ones in the rocks of the Dry Valley of Antarcticaand the Atacama Dessert (Friedmann 1982; Warren-Rhodes etal. 2006). The other research focus is on those living in theAtacama Desert, the driest place on Earth, demonstrating thatthe organisms indeed lived there and not just were blown infrom the air (Wettergreen et al. 2005; Drees et al. 2006).

Solvent resistance

Most microorganisms are killed by even small concen-trations (0.01%) of organic solvents such as toluene orchloroform, likely due to their lipid-destructive properties(Hirayama et al. 1998). In 1989, the first organic solvent-tolerant microorganism was isolated, a Pseudomonasthriving in high concentrations of toluene (Inoue andHorikoshi 1989). Many organisms now have been foundto tolerate 10% or even 50% toluene or other solvents, suchas kerosene, benzene, or various alcohols, though nonehave been found to require them for life (Sardessai andBhosle 2002; 2004), including extremophilic yeasts with

potential applications in biotechnology (Kaszycki et al.2006). There are several mechanisms which probablycontribute to this phenomenon: decreased influx viaremoval of solvent from cell membranes and/or physicalimpermeability (Heipieper et al. 1992; Pinkart et al. 1996),biochemical degradation or detoxification of the solvent(Ramos et al. 1997), active efflux of the solvent (Kieboomet al. 1998; Ramos et al. 1998), and overexpression ofgenes (Nakajima et al. 1995). It has been often noted that acorrelation between organic solvent tolerance and multipleantibiotic resistance exists, and perhaps the efflux systems,or at least their regulation, are similarly induced (Oethingeret al. 1998; Li and Poole 1999). The so-called multi-drugefflux systems of the Gram-negative pathogens have beenfairly well studied (Nikaido 1996; Paulsen et al. 1996), andit is noted that there is increased expression of these orsimilar operons in organic solvent-tolerant bacteria.

There has been much genetic investigation of organicsolvent-tolerant organisms, with certain genes believed tocontribute to or confer this property, depending on themechanisms employed. As would be expected, there doesnot appear to be a single, universal mechanism, but rather acombination of efflux systems, physical barriers to influx,and adaptation to the presence of the solvents. Bacillus andPseudomonas species have been found to possess thischaracteristic, though several solvent-tolerant E. coli strainshave been noted also, either naturally, via mutagenesis,under selective pressure, or via transformation with candi-date genes from tolerant species. Degrees of cell surfacehydrophobicity and/or membrane fluidity seem to correlatewith this tolerance and are seen to change with adaptationin the presence of solvents, likely affecting influx of thechemical (Aono and Kobayashi 1997; Tsubata et al. 1997).Some of the changes seen in adaptation to organic solventsare noted to be a general stress response in bacteria.

Organic solvent-degrading bacteria are interesting fortheir potential use in bioremediation, and obviously, thoseusing active efflux systems identical or similar to those usedby pathogens may have usefulness in the understanding ofantibiotic resistance. The study of these bacteria has yieldedmuch information on the toxicity of solvents to membranesystems in general. Worrisome is the possibility for selectionof multiple antibiotic resistance in pathogens by exposure tounrelated compounds such as pollutants and the fact that theresistance profiles of these organisms are then unrelated todrug type or site of action.

Resistance to low substrate concentration

In the open ocean, as well as in deep lakes, the first 100 to200 m of water are often illuminated, but contains scarcenutrients. Other habitats also exist which contain less than


20 mg/l organic carbonoligotrophic environments. It isin these habitats that oligotrophictrue members aredefined by their inability to propagate at elevated nutrientconcentrations (Conrad and Seiler 1982; Semenov 1991;Wainwright et al. 1991, 1993; Schut et al. 1997; Lauro et al.2009)organisms live and thrive. They grow under suchconditions by having highly effective systems for theuptake of inorganic and organic nutrients at nano- andpicomolar concentrations and by their efficient utilizationsystems characterized by unique metabolic regulation.Oligotrophs can be isolated from different natural sources,both with low and high concentrations of organic sub-stances, and those inhabiting soil and aquatic habitats areparticularly able to utilize geochemically important, lowmolecular organic and inorganic substances, which arerapidly processed but occur in very low concentrations.

Sphingomonas is an ultramicrobacterium which isadapted to oligotrophic habitats. Some strains have shownan enhanced ability to recover from UV-B radiation,perhaps adding to their ability to live and thrive in theupper water column where UV radiation exposure ismaximal (Joux et al. 1999). This organism also seems tohave a distinct response in transcriptional regulation intimes of starvation, which could point to further adaptationto depleted nutrients (Fegatella and Cavicchioli 2000).Recently, important insights were elucidated about cellstructure and metabolism in microorganisms belonging tothe Roseobacter and Collimonas genera which exhibitoligotrophic behavior (Leveau et al. 2009; Tang et al.2009).

Exobiology

In the search for extraterrestrial life, our closest neighborplanets are often considered as candidate habitats. The lackof surface water and extremely high surface temperature onVenus make it less likely than Mars as a source for life, butthe hygroscopic sulfuric acid clouds in the lower andmiddle cloud layers surrounding that planet, where thetemperatures are considerably lower, could be a favorableenvironment for acidophilic, sulfate-reducing, chemoauto-trophs growing as aerosols (Cockell 1999). Short of makingthe trip to look, further work on terran acidophiles may helpto clarify this possibility.

Understanding the biology of extremophiles and theirecosystems permits developing hypotheses regarding theconditions required for the origination and early diversifi-cation of life on a planet including Earth, the possibility ofpanspermia, and the potential habitats of past or present lifebeyond Earth in the solar system (on the planet Mars andthe Jovian moon Europa; some authors also suggestpossible habitats on other icy satellites, in Venus clouds,

and on the Saturnian moon Titan), or even in exoplanetarysystems. Recently, the introduction of novel techniquessuch as Raman spectroscopy into the search of life signs inextremophilic environments (Villar and Edwards 2006;Edwards et al. 2007; Alajtal et al. 2009) has open furtherchances and issues that might be very useful in exobiology,particularly for the development of unmanned remotelyoperated vehicles.

Among early microorganisms, cyanobacteria played amajor role, inventing oxygenic photosynthesis andcausing the most profound alteration of our planet.Cyanobacterial cell walls are commonly covered by S-layers or by carbohydrate structures forming slime orsheaths. They are composed of complex polysaccharidesand pigments like scytonemin (Hoiczyk and Hansel2000). These extracellular fibrillar carbohydrates providea protective coat for the cells against UV radiation anddesiccation as they maintain the cells in a highly hydratedgel-like matrix, permitting these organisms to adapt toextreme temperatures and desiccation, as in todays Antarc-tica, but probably also in early Earth environments (Olsson-Francis et al. 2010). After that, the presence of water on Marsand perhaps on some other planets and their moons has beenproven, and extra terrestrial life has become much morepossible than before, but the final judgment will beobtained when microorganisms are going to be isolatedfrom aseptic collected samples (Zolensky 2005; McSween2006).

In Antarctica, Lake Vostok is buried under almost4,000 m of ice and could serve as a model for thehypothetical ocean under the ice of Europa (Cavicchioliand Thomas 2000; Marion et al. 2003). Technologies arebeing developed to sample the lake ice and water withoutintroducing surface microbes and could be used in thefuture on Europa ice or Mars polar caps with respect toplanetary protection issues. Studying cold environmentssuch as ice, rocks of the Antarctic Dry Valleys, andpermafrost is also interesting for detecting new types ofpsychrophiles, as well as for studying preservation ofmicrobes. Microorganisms (prokaryotic and eukaryotic)can live in rocks (endoliths) or in sediments of Antarcticaand Arctic (Friedman et al. 1988; Sun and Friedmann 1999;Skidmore et al. 2000; Wynn-Williams and Edwards 2000;Siebert et al. 1996), in porosity of impact-shocked rocks(Cockell et al. 2002), and on bare rocks of hot desert (desertvarnish) (Gorbushina 2003; Edwards 2004). Besides bacte-ria, cryptoendolithic merismatic microfungi live in theporosity of rocks of the Antarctic Dry Valleys. These fungitolerate hard dessication, high UV exposure, extremely lowtemperatures, and wide thermal fluctuations (Onofri et al.2004).

The elevated resistance of microorganisms to extremeconditions, including most of that characterizing space


environments, led in the last two decades to several inves-tigations based on either manned or unmanned space vehiclesand modules, particularly the MIR station, the InternationalSpace Station, PHOTON, and BION capsules (Horneck et al.2001; Rettberg et al. 2004; Sancho et al. 2007; van Benthemet al. 2009). This was possible due to developments ofspatial technologies allowing the study of adaptations andsurvival of terrestrial organisms to vacuum, microgravity,and cosmic radiations; moreover, this expansion of humanactivities to space raised new issues related to microbiology,such as the development of life-support systems for futureplanetary stations, the control of biocontamination inconfined habitats, as well as planetary protection anddevelopment of strategies to prevent, detect, and labelterrestrial contaminants of extraterrestrial environments.

The deep subsurface biosphere includes chemolithotro-phic microbes in anoxic reducing environments underoceans and continents, in deep subsurface sediments, inhydrocarbon and water reservoirs, and in subsurface cavesas nicely reviewed by Teske (2005). Analogue habitats inwhich life is protected from harsh surface conditions areprobably common in other planets with some geothermalactivity, such as Mars.

Studying the biology and ecology of extremophiles isessential for defining the limits of life as we know ittheenvelope of lifeas well as for studying the preservation ofbiosignatures in extreme environments analogous to that ofearly Earth and/or to potential extraterrestrial habitats andfor testing technologies to detect them (Fendrihan et al.2009; Orange et al. 2009). One caveat might be that onEarth extreme environments are fed by nutrients fromnormal environments brought by winds, rains, etc.Therefore, the question arises as to whether or not a planetwith only extreme conditions might sustain life. Neverthe-less, not all extremophilic adaptations are derived con-ditions, and at least some of the anaerobic metabolisms areancestral.

Conclusions

Environments with extreme physicochemical parameterswere thought of as being hostile to life until microbiologistsdiscovered that they are actually inhabited by a widediversity of microorganisms. Organisms that survive andthrive under conditions that are detrimental to the majorityof the currently described species have become a focus ofincreasing scientific attention over the last few years, withsome groundbreaking discoveries of stress-toleratingmechanisms. Extremophiles are certainly promising modelsto expand our understanding of the functional evolution ofstress adaptation and maybe they will lead us to explore abiodiversity so far unrevealed.

We have described an updated overview over the mostrepresentative microorganisms living in environments hos-tile to most of eukaryotic forms of life. Understanding theevolution of microorganisms in extreme environments willincrease our basic knowledge of evolutionary processes andallow a better evaluation of the potential ecologicalconsequences of environmental changes.

If, as we believe, extreme environments are importantfor evolutionary processes, human activities may influencebiodiversity even more than previously thought and, aftermillennia of microbial evolution, the stability of thesefragile environments are in danger.

Future research directions, including the refinement ofculture media, strategies based on cellcell communication,high-throughput innovations, and a combination of theseapproaches, will lead to novel insights into the world thatonce was thought not to harbor any form of life.

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