geomicrobiology: its significance for geology

Ž .Earth-Science Reviews 45 1998 45–60

Geomicrobiology: its significance for geology

Henry L. Ehrlich )

Department of Biology, Rensselaer Polytechnic Institute, Troy, NY 12180-3590, USA

Received 21 October 1997; accepted 12 August 1998

Abstract

Some microorganisms, including various kinds of bacteria, fungi, algae, and protozoa, serve as geochemical agents in theuppermost lithosphere and in the hydrosphere. Some promote rock weathering by mobilizing mineral constituents withinorganic or organic acids or ligands that they excrete. Others promote rock weathering by redox attack of mineralconstituents such as Fe and Mn. Still others cause active or passive mineral formation by precipitation and subsequentnucleation of crystal formation on or in the cell, or in the bulk phase. They play a role in some phases of fossil fuelformation and accumulation. They modulate the terrestrial and marine cycles of C, N, S, and P and some other elements, andthey influence the composition of the atmosphere in respect to O , CO , and CH . Some discriminate between stable2 2 4

isotopes of H, C, O, N, and S. q 1998 Elsevier Science B.V. All rights reserved.

Keywords: atmosphere-composition; microorganisms-geochemistry; minerals-synthesis; weathering-process

1. Introduction

The aim of this article is to bolster awarenessamong geoscientists, as well as among microbiolo-gists and biologists in general, of some of the impor-tant roles that certain microbes have played and areplaying as geologic agents. An earlier article by the

Ž .author Ehrlich, 1996a , although touching on someof the topics covered herein, only emphasized themicrobial role in mineral growth and dissolution.However, microbes exert other geochemical influ-ences as well, as in their partial control of atmo-

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spheric composition, in the cycling of organic andinorganic matter and affecting its global distribution,in peat, coal and petroleum genesis, and in theirgeneral role in keeping the planet habitable for allforms of life.

2. Microbes and the evolution of the Earth in thePrecambrian

It seems certain that since the early Precambrian,the activity of microbes has had an impact on theevolution of the Earth’s surface, including the upper-most lithosphere and the hydrosphere. Microbial ac-tivity has also had an impact on the composition ofthe atmosphere. It is now generally accepted thatbacteria of various kinds were the only forms of life

0012-8252r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved.Ž .PII: S0012-8252 98 00034-8

( )H.L. EhrlichrEarth-Science ReÕiews 45 1998 45–6046

on Earth during the Precambrian, from about 4 eonsago, when cellular life is thought to have originated,to about 2 eons ago. The Earth is estimated to be 4.6eons old. The evidence for the existence of earliestlife rests mainly on carbon isotope data from thebanded iron formation in the Isua supracrustal belt in

Ž .West Greenland Mojzsis et al., 1996 and on thediscovery of prokaryotic microfossils from the EarlyArchean Apex Basalt in the northwest of Western

ŽAustralia, estimated to be about 3.5 eons old Schopf,.1983, 1993 , and the earliest eukaryotic fossils,

megascopic algae in the Negaunee Iron-Formationnear Marquette, MI, estimated to be about 2.1 eons

Ž .old Han and Runnegar, 1992 . These age estimatesof early life are also consistent with inferences drawnfrom phylogenetic studies using the techniques of

Ž .molecular biology Woese, 1987 . The earliest mi-crofossils were recognized as remains of bacterialmicrobes because their shapes appear similar to thoseof currently living bacteria. Because of this resem-blance, it has been inferred that these ancient mi-crobes must have had a complexity in cellular struc-ture and function close or equivalent to that of theirmodern counterparts and that they evolved fromprimitive ancestors existing hundreds of millions ofyears earlier.

Precisely how early microbes affected their envi-ronment we can only surmise from knowledge aboutthe activities of their modern counterparts, but therecan be no doubt that they had some effect. Since theorganic structure of all cells involves compounds ofpartially to nearly fully reduced carbon, the ancientmicrobes must have had an effect on the distributionof carbon at the Earth’s surface, and on its cyclingwhen the supply of carbon became limiting. Andsince the chemical structure of some of the differentcarbon compounds must also have included nitrogen,sulfur, andror phosphorus, these microbes must alsohave affected the distribution of these elements andtheir cycling when their supply became limiting. Asmicrobial metabolism became increasingly diverseand complex and a need arose for obtaining energywith greater efficiency and from heretofore untappedsources for growth and reproduction, microorgan-isms evolved with an ability to conserve energy from

Ž . Ž .sunlight phototrophy Deamer, 1997 and from theoxidation or reduction of certain inorganic elementsthat can exist in more than one oxidation state

Žchemolithotrophy and anaerobic respiration, respec-.tively , such as H, N, Fe, S, Mn and perhaps some

Ž .others in this category see Ehrlich, 1996b . At thesame time, phototrophs and lithotrophs learned to

Ž .form reduced organic carbon from CO . Previ-2

ously, metabolism was based mostly on consumptionof abiotically formed organic molecules. Thesemetabolic innovations had an even greater effect onthe distribution and cycling of various elements thanhad microbial activity before. The emergence of

Žoxygenic photosynthesizing microbes cyano-. Ž .Žbacteria formerly called blue-green algae Awra-

.mik, 1992 , which reduced CO with H O by a2 2

light-driven reaction:

H OqCO ™ CH O qO 1aŽ . Ž .2 2 2 2

led in time to a conversion of the primordial atmo-sphere into one in which O was the most dominant2

component after N over a period from about 3.5–32

eons to about 2 eons ago.By inferring that Early Precambrian microbes were

bacterial, it is implied that they possessed a prokary-otic cell organization. Typical prokaryotic cells aredelimited by a wall or cell envelope overlying a cell

Žmembrane that encloses the cell interior see Atlas,.1995, pp. 51–83 . These cells contain their genetic

information encoded in deoxyribonucleic acidŽ .DNA , which is not membrane bound as in eukary-otes. DNA determines what a cell is and does. Inprokaryotes, key physiological processes like photo-synthesis and respiration are not compartmentalizedin special intracellular organelles, as in eukaryotes.

Eukaryotic cells are delimited by a plasma mem-brane that may or may not be covered by a cell wall.Their primary genetic information is encoded in theDNA of chromosomes in a membrane-bound vesicle,the nucleus. Photosynthetic activity is compartmen-talized in chloroplasts, and energy-conserving activ-

Žity, from the oxidation of organic compounds respi-. Žration , is compartmentalized in mitochondria see

Atlas, 1995, pp 51–83; Lehninger, 1975, pp. 381–.382 . It must be noted, however, that the overall

nature of compartmentalized processes of eukaryotesis the same as similar uncompartmentalized pro-cesses in prokaryotes, although differing in somedetails. Compartmentalization apparently allowed for

( )H.L. EhrlichrEarth-Science ReÕiews 45 1998 45–60 47

subsequent evolution of complex multicellular plantsand animals with extensive division of labor amongthe cells arranged in tissues for optimal efficiency ofthe whole organism.

Eukaryotic cells did not arise de novo. Theyoriginated in the last third of the Precambrian fromsome non-specialized prokaryotic cells that were in-vaded by another prokaryotic cell specializing in

Žoxygen-utilizing respiration Margulis, 1970; Dod-.son, 1979 . The invaders, which benefitted the host,

in time lost their capacity for independent existenceand gradually evolved into the mitochondria found inmodern eukaryotic cells. Some of the non-special-ized prokaryotic cells were also invaded by prokary-otic cells specializing in oxygen-generating photo-synthesis, i.e., by a type of cyanobacterium, whichgradually evolved into chloroplasts found in moderneukaryotic photosynthesizers. Mitochondria andchloroplasts have retained some genetic informationŽ .DNA from their prokaryotic ancestors, which is notpart of the nucleus, but which is needed togetherwith information in the nucleus for their replication

Ž .and function Dyson, 1978 . The mode of replicationof this DNA is very similar to that in bacteriaŽ .Metzenberg and Agabian, 1994; Backert et al., 1996

While the prokaryotic microbes have continued toexert their extensive influence on the distribution ofmatter at and near the Earth’s surface to the presentday, the emergence and establishment of eukaryoticmicrobes and higher life forms evolving from themadded another important influence.

Whereas in eukaryotic cells, respiratory activityfor generating metabolic energy resides characteristi-cally in the mitochondria, in prokaryotic cells it isassociated with the plasma membrane and the cell

Ž .envelope see Atlas, 1995 . This location in prokary-otes enables some of them to oxidize or reducerelatively large quantities of metals and metalloidswith the appropriate enzymes without these sub-strates having to enter the cell interior where they

Ž .could poison the cell Ehrlich, 1996b . In eukaryotes,metals and metalloids would have to enter the cellinterior if mitochondria could promote large-scaleoxidation or reduction of them. Species of elementsthat bacteria are known to oxidize enzymaticallyinclude reduced forms of H, C, P, S, V, Mn, Fe, Co,

ŽCu, As, Se, Mo, Sn, Sb, W, and U Silverman and.Ehrlich, 1964; Ehrlich, 1996b . Species of elements

that bacteria are known to reduce enzymatically in-clude oxidized forms of C, P, S, V, Cr, Mn, Fe, Co,

ŽAs, Se, Br, Mo, Sb, Bi, Te, Hg, W, and U Woolfolkand Whiteley, 1962; Silverman and Ehrlich, 1964;

.Ehrlich, 1993, 1996b . Many if not all of these redoxcapacities probably arose during Precambrian evolu-tion. It is noteworthy that while a number of differ-

Ž .ent bacteria have been shown to reduce Cr VI in theŽ .form of chromate and dichromate to Cr III , some

aerobically, others anaerobically, none have beenŽ .shown to date to catalyze oxidation of Cr III to

Ž . Ž . Ž .Cr VI Ehrlich, 1996b . The oxidation of Cu I toŽ .Cu II by intact cells has been shown only when

ŽThiobacillus ferrooxidans attacks Cu S Fox, 1967;2.Nielsen and Beck, 1972 . The organism oxidizes the

Ž .Cu I before the sulfide–sulfur. Bacterial growth atŽ . Ž .the expense of the oxidation of Sn II to Sn IV has

Ž .so far not been observed Lewis and Miller, 1977 ,Ž .nor has growth at the expense the oxidation of U IV

Ž .to U VI to the best of my knowledge. However,energy conservation and CO fixation at the expense2

Ž . Žof U IV oxidation has been demonstrated DiSpirito.and Tuovinen, 1982 . No energy is conserved in the

Ž . o Žbacterial reduction of Hg II to volatile Hg Robin-.son and Tuovinen, 1984 , yet this reduction appears

to be an important mechanism by which bacteria canrid their environment of toxic mercury. In the case ofsome of the other elements that are listed, it stillremains to be determined whether growth is sup-ported by their oxidation or reduction. The physio-logical as well as environmental significance in to-day’s world of bacterial oxidation of hypophosphateand phosphite to phosphate, and the bacterial reduc-tion of phosphate to phosphite, hypophosphite orphosphene is not well understood. However, as awhole, biologically catalyzed redox reactions involv-ing inorganics have been and are presently the basisof some important degradative, diagenetic and authi-genic mineral transformations in the sedimentaryenvironment.

3. Geologic processes affected by microbes

Rock and mineral weathering is one process inwhich microbes very often play an important role bypromoting mineral diagenesis and dissolution. In


some instances, their weathering action may be dueto formation of metabolic products, especially whenthe microbes live in a film on the surface of a rockor mineral. In other instances, their weathering ac-tion may be the result of oxidative or reductiveattack of appropriately reactive mineral constituentsŽ .e.g., Fe, Mn, sulfide, sulfate of a rock or mineralŽ .Ehrlich, 1996b . All types of igneous and sedimen-tary rocks are susceptible to microbial weathering,

Žincluding siliceous silica, silicates, and aluminosili-. Ž .cates and calcareous carbonate rocks.

Mobilization of mineral constituents in weather-ing by microbes can be a selective process, i.e., onlyone or a few of the constituents of a mineral aredissolved. When this happens, the undissolvedresidue becomes enriched in the constituents notmobilized by the microbes.

3.1. Rock weathering by metabolic products of mi-crobes

Some microbes excrete chemical agents that cor-rode the rock through chemical interaction, or byoxidizing or reducing a rock component that leads tomineral diagenesis or dissolution. These chemicalagents may include the inorganic acids HNO and3

H SO and organic acids such as citric, oxalic and2 4

gluconic acids, produced mainly by fungi, and formic,acetic, lactic, pyruvic, succinic, 2-ketogluconic andsome other acids produced by bacteria. Microbesmay also excrete ligands such as ferric iron-complex-ing siderophores produced by bacteria and fungi, andlobaric and physolic acids produced by lichens, whichpromote rock weathering. Oxidative or reductiveweathering agents, produced mainly by bacteria, in-clude ferric ion produced by acidophilic iron bacte-ria, and sulfide produced by sulfate reducing bacte-ria. Ferric iron in acid solution attacks mineral sul-

Ž .fides such as CuS Sullivan, 1930 :

CuSq2Fe3q™Cu2qq2Fe2qqS0 1bŽ .

Ž .Sulfide reduces MnO Burdige and Nealson, 1986 :2

MnO qHSyq3Hq™Mn2qqS0 q2H O 2Ž .2 2

Although the role of corrosive agents in chemicalweathering of rock has been long recognized by

Ž .geologists Jones et al., 1981 , it seems still insuffi-ciently appreciated that microbes are dominantsources of these weathering agents or act as catalystsin the weathering process. Results from recent labo-ratory experimentation on the effects that solutions

Ž .of various organic acids reagent grade such aslactic, pyruvic, citric and oxalic acids have on rockminerals are still discussed as though in nature these

Žreactions were purely abiotic e.g., Wieland and.Stumm, 1992 . They are not when consideration is

given to the natural source of these acids. If certaincorrosive anthropogenic pollutants are disregarded,the large majority of the weathering reactions wouldnot occur in nature without microbes because nearlyall the weathering agents are metabolic end-productsformed by bacteria, fungi, or lichens from naturallyoccurring organic or inorganic substances, includingsome non-corrosive pollutants, deposited on or ab-sorbed by the rock.

Ž .Microbes bacteria, fungi, lichens that cause rockweathering by excretion of corrosive agents oftengrow on the surface of the rock in the form of abiofilm or colony. This growth habit can result inaccumulation of a relatively high local concentrationof the corrosive agent. This concentration will beaffected by the number of organisms producing it, bythe timing and rate of its production, and by thetendency of the reagent to become diluted in theextracellular environment. When the microbial popu-lation producing a weathering agent is not attachedto the rock, the production of the agent must besustained and the rate high to counteract its dilutionand thus its lessened effectiveness.

For a rock or mineral, bathed in water containingoxygen, to be weathered by sulfide or fermentationacids that are only formed under reducing conditions,

Ž .a thick biofilm ;10 mm has to develop on therock or mineral surface. The biofilm will consist of aconsortium of bacteria in which the organisms at theouter surface of the biofilm may be strict aerobes or

Žfacultative organism able to grow with or without.oxygen . If the organisms at the outer surface are

aerobes, facultative aerobes are likely to be locatedbelow them. The organisms at the bottom of thebiofilm next to the mineral surface will be anaerobesthat produce the weathering agents. The aerobes and


facultative aerobes above them establish an oxygen-gradient over the depth of the biofilm by consumingoxygen in their respiration at a faster rate than it canbe replaced by inward diffusion within the biofilm,thereby creating conditions at the bottom of the

Žbiofilm that support anaerobic metabolism Marshall,.1984; Charaklis and Marshall, 1990; Dexter, 1995 .

If the water bathing the rock or mineral containssufficient sulfate, the anaerobes at the bottom of sucha biofilm may be sulfate-reducing bacteria that pro-duce corrosive sulfide. In the absence of a significantsulfate concentration, the anaerobes may include fer-menters, which form corrosive organic acids as well

Žas CO Huang and Keller, 1972; Bennett et al.,2.1988; Welch and Ullman, 1993 .

In some unpolluted, dry environments, includingdeserts, lichens are important actors in weathering of

Ž .rock surfaces Ferris et al., 1989 . Except for someŽendolithic forms in the Antarctic dry desert Fried-

mann, 1980; Friedmann and Ocampo-Friedmann,.1984 , they are a structurally highly organized con-

Žsortium, consisting of a photobiont either an alga or. Ž .a cyanobacterium and a mycobiont fungus that are

Ž .physiologically interdependent Ahmadjian, 1967 .The mycobiont of typical lichens usually enclosesthe photobiont, shielding it from excess sunlight aswell as sharing mineral nutrients which it absorbsfrom the rock stratum being weathered. The photo-biont shares with the mycobiont the organic carbon itsynthesizes in CO -assimilation driven by the chemi-2

cal energy derived by transduction of radiant energyabsorbed from sunlight. In endolithic forms inAntarctica, the photobiont grows close to the surfacein the rock to receive light energy for photosynthesis.It is accompanied by the mycobiont, which alsogrows slightly deeper in the rock because it is not

Ž .dependent on sunlight Friedmann, 1980 . Lichensproduce ligands that extract mineral constituents fromthe rock being weathered. Examples of such ligandsare oxalic, lobaric and physolic acids, which can

Žcomplex iron and other mineral constituents Schatz,.1962; Ferris et al., 1989; Johnston and Vestal, 1993 .

Microbial weathering of rock has a practical as-pect that has been under-appreciated. This aspect ofweathering is involved in the deterioration of naturalbuilding stone and concrete, and stone sculpturesŽPaine et al., 1933; Lyalikova and Petushkova, 1991;Palmer and Hirsch, 1991; Gorbushina et al., 1994;

.Blazquez et al., 1995 . Limestone and sandstone are´especially susceptible to this action. It takes placeafter naturally occurring organics from soil or non-corrosive pollutants in air are deposited on stone andtransformed into corrosive agents by the microbialflora inhabiting the surface and superficial pores of

Ž .the stone Urzı and Krumbein, 1994 . Microbes´growing in pores, minute cracks and fissures of stonemay also damage it physically through exertion of

Ž .pressure by their cell mass Gorbushina et al., 1994 .The growth of microbes on and in stone may lead to

Žits discoloration or a change in color Urzı et al.,´.1991 .

Concrete, an artificial stone, is subject to micro-bial attack leading to its structural failure, whether

Žreinforced or not Milde et al., 1983; Sand and Bock,.1991; Zherebyateva et al., 1991 . The collapse of

concrete sewers due to such microbial action hasbeen recorded on a number of occasions. In theseinstances, inorganic and organic sulfur in sewagewas turned into sulfuric acid by sulfur oxidizingbacteria, which then attacked the concrete.

3.2. Mobilization of metals in metal sulfides.

The chemical reaction in weathering of rocks andminerals by microbial metabolic products does notusually involve direct microbial catalysis. However,some weathering processes involving redox reactionsmay be directly catalyzed by microbes. An exampleis the mobilization of metals from metal sulfides.

Until 1947, geochemists believed that the mobi-lization of metals from sulfide minerals in naturewas an abiotic process, although Rudolfs had sug-

Ž .gested in 1922 Rudolfs, 1922 that sulfur-oxidizingbacteria might promote the oxidation of pyrite. When

Ž .in 1947, Colmer and Hinkle 1947 reported that ironoxidation associated with acid mine drainage forma-tion was biological, and when in 1950 Colmer et al.Ž .1950 announced the isolation of the first aci-dophilic, Fe2q and reduced-sulfur-oxidizing bac-terium from such drainage, that view gradually

Ž .changed. Temple and Colmer 1951 showed theirorganism to be an autotroph and named it T. ferroox-idans. It was held responsible for the generation ofacid mine drainage, together with Thiobacillus


thiooxidans, which was also detected in acid mineŽ .drainage Kleinmann and Crerar, 1979 . Whereas T.

ferrooxidans oxidizes both Fe2q and reduced formsof sulfur, T. thiooxidans oxidizes only reduced formsof sulfur. Since elemental sulfur and thiosulfate aswell as ferrous iron are recognized among the inter-mediates in pyrite oxidation, substrates for both or-ganisms occur. Evidence now indicates that T. fer-

Žrooxidans attacks pyrite itself Murthy and Natara-jan, 1992; Mustin et al., 1992; Nordstrom and

.Southam, 1997 . The critical overall reactions thatdescribe the role of T. ferrooxidans in the formationof acid mine drainage have been briefly summarized

Ž .and discussed by Ehrlich 1996a,b . The thiosulfateand sulfur, which T. thiooxidans needs for its growthand which T. ferrooxidans can also oxidize, may

3q Žresult from the attack of pyrite by Fe Schippers et.al., 1996 :

FeS q6Fe3qq3H O™7Fe2qqS O2y q6Hq2 2 2 3

3Ž .

2S O2y q2Fe3q™S O2y q2Fe2q 4Ž .2 3 4 6

T . ferrooxidans2y 2y 2yS O qH O ™ S O qSO4 6 2 2 3 4

qS0 q2Hq 5Ž .

The discovery to T. ferrooxidans in acid coalmine drainage and its role in acid drainage formationsoon led to its identification in acid mine drainagefrom metal sulfide deposits, especially from copper

Ž .sulfide deposits Bryner et al., 1954 . The ability ofthe organism to promote oxidation of various metalsulfides, including those of Co, Ni, Mo, Pb, and Zn

Žamong others, was soon demonstrated Bryner andAnderson, 1957; Bryner and Jameson, 1958; Ivanovet al., 1961; Malouf and Prater, 1961; Ivanov, 1962;Razzell and Trussell, 1963; Torma, 1971; Silver and

.Torma, 1974 .Ž .Using CuS covellite as an example, T. ferrooxi-

dans may directly catalyze the oxidation of the metalŽsulfide according to the reaction Silverman and

.Ehrlich, 1964 :

CuSq2O ™Cu2qqSO2y 6Ž .2 4

or indirectly with Fe3q that the bacteria generate byŽ .oxidizing pyrite Silverman and Ehrlich, 1964 :

CuSq2Fe3q™Cu2qq2Fe2qqS0 7Ž .

The resultant S0 will be further oxidized to sulfateby either T. ferrooxidans or T. thiooxidans:

S0 q1.5O qH O™2HqqSO2y 8Ž .2 2 4

Fe3q is not a strong enough oxidant to convert S0

into sulfate abiotically.T. ferrooxidans is not the only acidophilic bac-

terium capable of oxidizing Fe2q, reduced sulfur,and metal sulfide. Since its discovery, a number ofother acidophilic bacteria have been found, some ofwhich, like T. ferrooxidans, grow in a temperature

Ž .range from around 15–408C mesophilic , while oth-ers grow in a higher temperature range of 40–758CŽ .thermophilic . Among them are the mesophile Lep-tospirillum ferrooxidans, and the thermophiles Sul-fobacillus thermosulfidooxidans, Acidianus brier-leyi, Sulfolobus acidocaldarius, and others. T. fer-rooxidans, L. ferrooxidans and S. thermosulfidooxi-dans are eubacteria, whereas A. brierleyi and S.acidocaldarius are archaea. For a more detailed dis-cussion of the physiology of these and other aci-

Ž .dophilic iron-oxidizers, see Ehrlich 1996b .One or more of these acidophilic iron-oxidizers

can be found naturally at sites where metal sulfidesoccur, such as in bituminous coal seams with pyriteinclusions, and in metal sulfide ore deposits. Unlessthe deposits containing metal sulfides are exposed toair and significant moisture, the bacteria are eitherdormant or only weakly active. But when pyrite-con-taining coal seams or metal sulfide ore depositsbecome exposed as a result of a seismic or othernatural happening, or in mining activity, the bacteriamay become very active and grow, resulting in theformation of acid mine drainage. In the case of metalsulfide ore deposits, this activity can be and isindustrially exploited for metal recovery withoutsmelting in a process called biohydrometallurgyŽLundgren and Malouf, 1983; Ehrlich and Brierley,

.1990; Ehrlich, 1996b . Such exploitation merely re-quires the stimulation of the bacteria already presentby watering and aerating a fractured or rubbilizedsulfide ore deposit in situ, or after placing the minedore in dumps or heaps. If the ore contains significant


carbonate inclusions, at least the initial water mayhave to be acidified to overcome the neutralizingaction of the carbonate. Since the bacteria are au-totrophs, no organic nutrients are required.

3.3. Mineral deposition

Microbes also play a role in authigenic or diage-netic formation of certain minerals or sedimentaryrock. Examples of authigenic microbial mineral for-mation are the oxidation of dissolved ionic species,such as Fe2q to Fe O , Mn2q to MnO or other2 3 2

Ž . y 0manganese IV oxide, HS to S , or the reduction of2y Ž . ŽCrO to CrO OH see discussion by Ehrlich,4.1996b . Stibiobacter senarmontii may oxidize Sb O2 3

Ž .to Sb O Lyalikova, 1974 , and Geobacter metal-2 5

lireducens GS-15 may reduce MnO to MnCO2 3Ž .Lovley and Phillips, 1988 . An example of diage-netic mineral formation is the replacement of carbon-ate in calcite by phosphate mobilized in the micro-bial degradation of phosphorus-containing organic

Ž .matter Hirschler et al., 1990a,b .Although clays have been generally viewed as

being formed abiotically by diagenetic transforma-tion of some igneous minerals and preexistent clays,evidence for authigenic clay formation under envi-ronmentally compatible conditions was presented re-

Ž .cently Urrutia and Beveridge, 1995 . In this study,allophane was formed on the surface of non-growingcells of Bacillus subtilis strain 168, incubated insolutions containing various combinations of Al, Si,Zn Cd, tannic, citric and fulvic acids. The bacteriacaused a rise in pH of the reaction mixtures andcounteracted the inhibitory effect of citric, tannic andfulvic acids on allophane formation in their absence.

Microbes have been implicated for some time inŽthe deposition of some iron minerals e.g., Cloud,

1973; Lundgren and Dean, 1979; Walker et al.,1983; Nealson and Myers, 1990; Ghiorse and Ehrlich,

.1992; Schwertmann and Fitzpatrick, 1992 . An ob-servation suggesting a microbial role in formation ofsome iron deposits has been the finding of fossilizedremains of cyanobacterial or alga-like organisms in

Žsuch ore Gruner, 1923; Cloud and Licari, 1968,.Ghiorse and Ehrlich, 1992 . In the case of cyanobac-

teria and algae growing in mats in shallow bodies ofwater, their photosynthetic activity can lead to theprecipitation of iron oxides around them. Continuedaccumulation of the oxides in the mat results in the

build-up of a deposit. The following reactions associ-ated with cyanobacteria or algae may have beenresponsible for the iron precipitation:

2HCOy lCO qCO2y qH O 9Ž .3 2 3 2

light, chlorophyllCO qH O ™ CH O qO 10Ž . Ž .2 2 2 2

CO2y qH OlHCOy qOHy 11Ž .3 2 3

2Fe2qq0.5O q3H O™2FeO OH q4HqŽ .2 2

12Ž .Ž .In this scheme, reaction 10 is rate-limiting and

controls the overall process of iron deposition bymaintaining a circumneutral to alkaline environment

Ž .in the cyanobacterial or algal mat via reactions 9Ž .and 11 , and by generating an excess supply of

oxygen that favors iron autooxidation via reactionŽ .12 . Iron autooxidation becomes negligible belowpH 5.0.

Ochre formation has been associated with ap-pendaged bacteria like Gallionella ferruginea, andsheathed bacteria like Leptothrix ochracea and L.discophora. The first is known to oxidize Fe2q

under partially reduced conditions, i.e., at low O2Ž y1 . Ž .tension 0.1–1 mg l Hanert, 1981 . It deposits

the oxidized iron in its lateral stalk. The second ofthe two organisms may oxidize Fe2q with an extra-cellular enzyme under conditions where iron autoxi-dation is slow, accumulating the ferric iron in its

Žsheath Corstjens et al., 1992; Ghiorse and Ehrlich,.1992 .

A number of investigators have associated theorigin of freshwater and marine manganese noduleswith bacterial activity. Most freshwater concretionsdiffer structurally and mineralogically from marine

Žconcretions Ghiorse and Ehrlich, 1992; Ehrlich,.1996b . In the case of concretions on the bottom of

parts of Lake Oneida, NY, mats of the cyanobacte-rium Microcystis have been implicated as an agentof manganese oxidation in surface waters. On thedeath of the cyanobacteria, the oxidized manganeseis carried to the lake bottom by the settling biomass

Žand incorporated into concretions Richardson et al.,.1988 . Manganese-oxidizing bacteria have also been

detected in the bottom waters of the lake and arebelieved to contribute oxidized manganese to the

Ž .concretions Chapnik et al., 1982 .At least three kinds of manganese-oxidizing bac-

teria have been associated with the growth of marine


Ž .manganese nodules Ehrlich, 1996b . One kind bindsoxidized manganese in slime at the cell surface, andthen initiates nodule formation by cell aggregationŽ .Kalinenko et al., 1962 . Another kind has beenshown in laboratory experiments to bind freely dis-solved manganese in seawater to its cell surface and

Ž .oxidize it Kepkay et al., 1984 . A third kind oxi-dizes Mn2q after the manganese has first been boundto preformed ferromanganese oxide or certain clays.This last type has been shown to be able to deriveenergy from the oxidation, although it is not au-totrophic. Its mechanism of action also explains besthow bacterial manganese oxidation contributes di-

Ž .rectly to nodule growth see Ehrlich, 1996b .The origin of some sedimentary carbonate de-

posits has been associated with microbial activityŽ .see Golubic, 1973; Pentecost, 1991; Ehrlich, 1996b .Some chalk deposits were formed by major accumu-lations of CaCO tests of calcareous foraminifera, a3

kind of amoeboid protozoan, others by accumulationof coccoliths from certain calcareous green algae,

Ž .and rhabdoliths Pettijohn, 1975 . It has also beenclearly established that a significant portion of theCaCO making up coral reefs was produced by3

coralline algae, the rest having been formed byanthozoan coelenterates, a group of invertebratesrelated to jellyfish. The remains of coccolithophores,and calcareous foraminifera, like Globigerina, arealso chief constituents of calcareous muds on someparts of the ocean floor.

CaCO deposition can also be promoted by bacte-3

ria. The role of sulfate-reducing bacteria, a group ofanaerobes, in causing the formation of secondarycalcite during reduction of sulfate derived from an-

Ž . Ž .hydrite CaSO or gypsum CaSO P2H O has been4 4 2

well established in studies of the origin of sulfurŽdomes and similar deposits see discussion by

.Ehrlich, 1996b . Some aerobic bacteria have alsoŽbeen implicated in CaCO deposition e.g., Green-3

field, 1963; McCallum and Guhathakurta, 1970;Krumbein, 1974; Morita, 1980; Newman et al.,

.1997a . These include heterotrophic bacteria thatmineralize organic carbon in a circumneutral envi-ronment rich in dissolved calcium. They also includecyanobacteria which generate carbonate in the con-sumption of bicarbonate in photosynthesis and

Ž Ž .thereby create alkaline surroundings see Eqs. 9 –Ž . .11 above , which favors the precipitation of the

carbonate by Ca2q dissolved in the water. AccordingŽ .to Thompson and Ferris 1990 , the cyanobacterium

Synechococcus converts intracellular HCOy photo-3Ž .synthetically into reduced carbon CH O according2

to the reaction:

HCOy qH O™ CH O qO qOHy 13Ž . Ž .3 2 2 2

The intracellular OHy is exchanged for extracellularHCOy across the cell membrane. The now extracel-3

lular OHy generates an alkaline pericellular regionwhere CO2y is generated from HCOy:3 3

HCOy qOHy™CO2y qH O 14Ž .3 3 2

The resultant CO2y reacts immediately with Ca2q at3

the cell surface to form CaCO . The calcite deposits3

of Synechococcus can be in the form of marl sedi-Ž .ment and massive bioherms Thompson et al., 1990 .

Some other cyanobacteria lay down CaCO as con-3Ž .cretions around pebbles in streams Golubic, 1973 .

An alternative explanation for CaCO formation3

in the case of the alga Chara corallina has beenŽ .offered by McConnaughey 1991 . According to him,

this alga lays down CaCO pericellularly according3

to the reaction:

Ca2qqCO qH O™CaCO q2Hq 15Ž .2 2 3

This reaction is driven by an energy consumingexchange of extracellular Hq for intracellular Ca2q.The Hq accumulated intracellularly protonates intra-cellular HCOy to form CO :3 2

HqqHCOy ™CO qH O 16Ž .3 2 2

which is needed for photosynthetic carbon fixationby reaction 10.

Some silica deposits, in particular siliceous oozes,are attributable to growth and activity of certain

Žalgae and protozoa Strahler, 1976; Werner, 1977;.Goldman and Horne, 1983 . In some marine sedi-

ments at mid-latitudes, siliceous remains of diatomsŽare found in major accumulations diatomaecous

.oozes . In some other marine sediments at low lati-tudes, siliceous remains of radiolaria, a kind of

Žamoebic protozoan, have accumulated radiolarian.oozes . Accumulations of siliceous remains of di-

atoms are also found in some freshwater sediments.Living diatoms and other siliceous algae as well assiliceous protozoans assimilate dissolved silicate,


preferentially as orthosilicate, and transform it into apolymer that forms the main component of the wall

Žstructure of the siliceous algae and the tests protec-.tive andror cell support structures of siliceous pro-

Ž .tozoans de Vrind-de Jong and de Vrind, 1997 .Microorganisms that promote weathering of silicate

Ž .rock see above play a significant role in keepingthe nutritionally required silicon available to organ-isms that need to assimilate it. Si-assimilating organ-ism include not only siliceous algae and protozoans,but also various plants, invertebrates and vertebrates.Ž .For further discussion see Ehrlich, 1996b

In addition to the highly structured siliceous andcarbonate structures formed by actively growing or-ganisms, mats of cyanobacteria may trap silicateandror carbonate and become silicified or embeddedin siliceous carbonate and finally fossilized as stro-

Žmatolites Walter, 1976; Cohen et al., 1984; Fried-.man and Krumbein, 1985 . The silicification does

not require active metabolism by the organisms in-volved, but carbonate deposition may. Cyanobacte-rial stromatolites are common in the later Precam-brian and early Phanerozoic fossil record but rare in

Ž .younger deposits Awramik, 1984 . Their rarity inthe later Phanerozoic fossil record has been at-tributed to the emergence of grazing and burrowinganimals that fed on the cyanobacterial mats. Theoldest known stromatolite is from the Warrawoona

ŽGroup in Western Australia Lowe, 1980; Walter et.al., 1980 . Modern stromatolites are found in only a

few special places such as some marine subtidalbasins and intertidal flats, thermal springs, somerivers, and some Antarctic lakes where the mats fromwhich they originate are not preyed upon by grazersŽ .Awramik, 1984 .

Microbes have been shown to be able to promotethe formation of minerals at moderate temperaturesand atmospheric pressure, previously thought to beformed only at high temperature and pressure. Theformation of various metal sulfides as a result ofreaction of metal ions with biogenic sulfide is a case

Žin point Miller, 1950; Baas Becking and Moore,.1961; Temple and LeRoux, 1964 . The recent

demonstration of the formation of the arsenic trisul-Ž .fide, orpiment As S , from arsenate and sulfate2 3

Ž .Newman et al., 1997b is another example. Bio-genic sulfide is formed anaerobically by reduction ofsulfate by sulfate-reducing bacteria. The sulfide then

reacts chemically with a metal or metalloid to formthe corresponding sulfide in the bulk phase. In thecase of the biogenesis of arsenic trisulfide, a specificorganism, Desulfotomaculum auripigmentum, was

Ž . Ž .required to reduce As V to As III and sulfate tohydrogen sulfide sequentially at rates that avoid ac-cumulation of an excess of sulfide. Lactate was theelectron donor in laboratory experiments. Living cellswere needed for nucleation of As S precipitate at2 3

circumneutral pH.Microbes can promote the build-up of a metallic

mineral at their cell surface by first binding the metalcation to negatively charged groups of the cell enve-lope. Such bound metal ions may subsequently reactwith anions to form an insoluble salt. The salt formsbecause it is more stable than the previous state inwhich the cation was bound to a cell envelopeconstituent. In sufficient excess of the requiredcations and anions, the metal salt on the cell surface

Žnucleates mineral formation Beveridge and Murray,1980; Doyle, 1989; Ferris, 1989; Schultze-Lam et

.al., 1996 . The anion in this reaction may be aŽproduct of bacterial metabolism e.g., Macaskie et

.al., 1987, 1992 , or it may have an abiotic origin.A somewhat different form of microbial mineral

nucleation was shown by Southam and BeveridgeŽ .1994 . They demonstrated in laboratory simulationthat a strain of B. subtilis, a common soil bacterium,

Ž 3q.immobilized auric gold Au intracellularly asŽ .small colloidal particles 5–50 nm . On autolysis of

the cells, these colloidal particles were transformedby re-solution followed by re-precipitation into pla-

Ž .nar pseudo-trigonal hexagonal –octahedral andhexagonal–octahedral gold crystals that aggregated

Ž .to form small placer-gold particles 50 mm whenincubating at 608C over a period of months.

3.4. Microbial isotope fractionation

Some microbes also have the ability to fractionateŽsome stable isotope mixtures for further discussion

.see Ehrlich, 1996b; Mortimer and Coleman, 1997 .The elements for which this has been experimentallydemonstrated include 12 Cr13 C, HrD, 14 Nr15 N,16Or18O, and 32 Sr34S. The operational basis for thismicrobial discrimination between stable isotopes of agiven element is kinetic, i.e., the reaction rates forthe different stable isotopes of a given element in a


key unidirectional reaction differ sufficiently for dis-crimination to occur. In bacterial sulfate-reduction,the key reaction that discriminates between 32 S and34S is the cleavage of the first S–O bond of sulfateŽ .see Hoefs, 1997 . In photosynthesis, the key reac-tions in discriminating between 2C and 13C are theuptake of CO into the cell and its subsequent2

fixation by the enzyme ribulose-bisphosphate-Ž .carboxylaseroxidase see Hoefs, 1997 .

3.5. Microbiology of the deep-subsurface

Microbial subsurface studies to date have shownŽthat in samples from the superficial subsurface 10 to

.50 m , viable bacteria, algae, fungi and protozoaŽmay be detected Ghiorse and Balkwill, 1983; Wil-

.son et al., 1983; Sinclair and Ghiorse, 1987, 1989 ,Žwhereas in samples from the deeper subsurface 150

.to 250 m in the Upper Atlantic Coastal PlainProvince on the east coast of the USA, mostlybacteria but few if any algae, fungi, or protozoa were

Ž .seen Sinclair and Ghiorse, 1989 . Below a depth of250 m down to several thousand meters, only viable

Žbacteria have been recovered to date Balkwill and.Boone, 1997; Stevens, 1997 . Most of the samples

examined in these surveys were from sedimentarydeposits. Successive strata in sedimentary deposits inthe Atlantic Coastal Plain Province, in which mi-crobes were numerous, varied in composition. Some

Žcontained sand andror silt, others were clayey e.g.,Sargent and Fliermans, 1989; Sinclair and Ghiorse,

.1989 .As at or near the surface, some microbes in the

deep subsurface may inhabit rock faces or the sur-face of mineral particles, occurring in biofilms, mi-crocolonies, or as individual cells. Other microbesmay occur preferentially in pore water. Those foundon rock or mineral surfaces are usually attached byslime that they produce. A significant number ofsuch microbes may not be culturable in the labora-tory. Their detection and enumeration depends onnewly developed molecular biological techniquesŽ .White and Ringelberg, 1997; Reeves, 1997 .

The rate of microbial metabolism in the deepsubsurface has been a matter of some dispute. Atpresent, a very slow rate, compared to metabolism atthe surface, is favored, based on some observations

Žand calculations Chapelle and Lovley, 1990; Kieft

.and Phelps, 1997 . In general, the rate of metabolismin the deep subsurface must be assumed to vary overtime depending on fluctuating nutrient availability.Such availability is likely to be limiting under thebest of circumstances.

Depending on the nutrient status of any subsur-face location, the bacteria may range from het-

Žerotrophs getting their carbon and energy from or-. Žganic matter to chemolithotrophs getting their car-

bon from CO and energy from the oxidation of2.inorganic matter . Thus heterotrophs would more

likely occur in significant number in sedimentarydeposits that contain trapped, metabolizable organiccarbon or are infiltrated with metabolizable organic-carbon-containing groundwater. Chemolithotrophswould more likely occur in rock deposits of igneousorigin in which organic carbon would have beendestroyed by the heat of the magma from whichthese rocks formed, but where inorganic energysources were available. But chemolithotrophs wouldalso be expected in some sedimentary deposits lowin organic carbon.

Depending on the oxygen content and the concen-tration of oxidizable organic matter of the pore wa-ter, the bacteria in contact with it may be aerobes,facultative aerobes, or anaerobes. They may resideon the rock or mineral surfaces as biofilm, micro-colonies, or individual cells, or they may residewithin the pore water. The aerobes can include het-erotrophic mineralizers of organic carbon; au-totrophic oxidizers of ammonia, nitrite, reduced sul-fur, and ferrous iron; and manganous-manganese-

Ž .oxidizing mixotrophs see Ehrlich, 1996b . Theanaerobes can include among others, fermenters,which require no externally supplied electron accep-tors in oxidizing their energy source, and nitrate-re-

Ž .ducers, ferric iron-reducers, manganese IV -re-ducers, sulfate- and sulfur-reducers, and CO reduc-2

Žers most methanogens, i.e., methane-forming bacte-.ria, and acetogens, i.e., acetate formers , which do

require corresponding externally supplied electronŽacceptors Lovley and Chapelle, 1995; Ehrlich,

Ž .1996b; see Odom and Singleton 1993 for moreŽ .information on sulfate reducers, and Ferry 1993 for

more information on methanogens and acetogens;.see also Section 3.6 . For the methane-forming bac-

teria, CO is the externally supplied electron accep-2

tor, except in the case of those which can degrade


acetate to methane and CO by a disproportionation2Ž .reaction really a special kind of fermentation :

0.5CH COOyqH O™CO q3.5Hqq4e 19Ž .3 2 2

0.5CH COOyq4.5Hqq4e™CH qH O 20Ž .3 4 2

Sum of reactions 19q20:

CH COOyqHq™CH qCO 21Ž .3 4 2

The organisms in contact with rock and mineralsurfaces in sedimentary strata of the subsurface canpromote gradual or rapid weathering of their sub-strate, depending on the nature of the rock or mineral

Žand the intensity of their metabolism Lovley and.Chapelle, 1995 . The CaCO of limestone would be3

very susceptible to dissolution by CO after conver-2

sion to H CO :2 3

CaCO qH CO ™2HCOy qCa2q 22Ž .3 2 3 3

regardless whether the CO derived from aerobic or2

anaerobic respiration or from fermentation. Anyacids, whether inorganic like nitric acid from ammo-nia oxidation via nitrite, or sulfuric acid from oxida-tion of reduced forms of sulfur, or any of a variety oforganic acids produced by subsurface microbes inconsumption of organic matter for energy produc-tion, would also be very corrosive. In the case oflimestone, such dissolution could increase the poros-ity of the limestone and contribute significantly tothe formation of vugs and caverns. Other rock types,both sedimentary, and igneous could also be attackedby the same corrosive agents as the limestone. Intheir attack, silicate and aluminum ions could buildup in the pore water.

If the groundwater has an appropriate compositionand pH, subsurface microbes could also cause repre-cipitation and possibly crystallization, of some thedissolved constituents. This in turn could lead to theplugging of pores and channels in subsurface de-posits.

3.6. Transformation of organic carbon in sediments

A significant portion of natural organic mattertrapped in sediment at the time of its deposition maysubsequently be only incompletely mineralized bymicrobes. This may be because of the nature of theorganic matter andror the lack of sufficient externalelectron acceptors required by microbes for the

Žbiodegradation process Alexander, 1977; Paul and.Clark, 1989 . Cellulose and, especially, lignins in

woody plant residues are difficult for microbes todegrade, especially anaerobically, and are likely toaccumulate only partially altered in the form ofhumic substances. Superficially buried, such organicmatter may become peat. Deeply buried and in largequantities, such residual organic matter may be fur-ther transformed into coal by physicochemical pro-cesses involving heat and pressure. Cyanobacterialand algal biomass trapped in sediments of shallowinland seas in the geologic past, and in at least onecase even now, has become gradually converted topetroleum hydrocarbons by physicochemical pro-cesses involving heat and pressure while new sedi-ment accumulated over the original deposit. A mod-ern example of petroleum genesis has been detected

Žin the Guaymas Basin, Gulf of California see sum-.mary of the work of Goetz and Jannasch, 1993 . In

other cases, where conditions permit, extensivebiodegradation of buried biomass in the absence ofoxygen may take place, the final products of thedegradation being mainly methane and carbon diox-ide, and some hydrogen. Final steps involvingmethane and carbon dioxide formation are repre-sented by reactions 19–21 above, and by the reac-tion:

CO q8H ™CH q2H O. 23Ž .2 2 4 2

Ž .The acetate for reactions 19–21 , and the H and2Ž .some of the CO for reaction 23 result from prior2

fermentation and anaerobic respiration of more com-plex organic matter by other anaerobic microbes.Some of the acetate may also result from acetogene-

Žsis by certain anaerobic, autotrophic bacteria Balch.et al., 1977; Eden and Fuchs, 1983; Fuchs, 1986 :

2CO q4H ™CH COOHq2H O. 24Ž .2 2 3 2

If escape of methane and carbon dioxide from thesediment into the atmosphere is naturally prevented,reservoirs of this gas mixture build up. In somecases, where such gas deposits are situated in coastalsediments, gradual seepage of the gases from ventsbelow sea level may cause the development of aspecial community around the mouth of the vents, inwhich the methane is the primary source of energyŽ .Cavanaugh et al., 1987; MacDonald et al., 1990 .Invertebrate animals such as certain worms and shell


fish, which have formed close symbiotic relation-ships with methane-oxidizing bacteria, live at theexpense of the methane. The bacterial symbiontsoxidize the methane and share some of the energythey conserve from this oxidation and perhaps someof the fixed carbon with their invertebrate hosts. Themethane-utilizing invertebrates thus form the bottomof a methane-based food chain.

4. Conclusion

It should be clear from the foregoing account thatmicrobes in promoting many geochemical processeshave exerted important controls on the distribution ofmatter in the upper lithosphere, the hydrosphere, andthe atmosphere since the Earth first formed. Theywill continue to do so in the future.

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Henry L. Ehrlich, Ph.D. holds the rankof Professor Emeritus in the Departmentof Biology of Rensselaer PolytechnicInstitute in Troy, NY, U.S.A. He servedon the faculty from 1951 until his retire-ment in 1994. He earned a B.S. degreein Biochemical Sciences from HarvardCollege in 1951, and an M.S. and aPh.D. degree in Agricultural Bacteriol-ogy from the University of Wisconsin,Madison in 1949 and 1951, respectively.He is a fellow of the American Academy

of Microbiology and of the American Association for the Ad-vancement of Science. He is also a member of the Interdisci-

Žplinary Committee of the World Cultural Council Consejo Cul-.tural Mundial . His research activities since 1959 have focused on

Ž .areas of geomicrobiology, including bacterial Mn II oxidationŽ .and Mn IV reduction related to marine ferromanganese concre-

tions, hydrothermal vents and some freshwater environments,Ž .bacterial interaction with metal sulfides bioleaching , bacterial

Ž .arsenite oxidation, bacterial Cr VI reduction, and bacterial inter-action with orthoclase and bauxite ore. He is the author of 3editions of a textbook on ‘‘Geomicrobiology’’ published by Mar-cel Dekker, New York. He co-edited the book ‘‘Microbial Min-eral Recovery’’ published by McGraw-Hill. He is the author orco-author of about 100 articles. He served as editor-in-chief of theGeomicrobiology Journal from 1983–1987, and is presently con-tinuing as co-editor-in-chief. He is also currently serving on theeditorial board of Applied Microbiology and Biotechnology. He isa founding member and has served as one of the Directors andTreasurer of the International Symposia on Environmental Bio-geochemistry, Inc. He continues to be active in research, writingand journal editing.

geomicrobiology: its significance for geology

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