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1321 The CanadtonMincralo gist Vol. 33, pp. 132l-1333 (1995) A REVIEWOF THEMICROBIALGEOCHEMISTRY OF BANDEDIRON.FORMATIONS D. ANNBROWN Departnewof Geolnglcal ManitobaR3T2N2 Scienres, Univenityof Manitoba,Vtliw1ipsg, GORDONA. GROSS Geological Suneyof Canada, 601BoothSteet,Ottawo,OwarioKIA 0E8 JERZYA. SAWICKI AECI" Chalk Riverlaboratories, ChalkRiver, Ontario KOJ1J0 Ansrnesr The role of micrmrganirms in the depositionof bandediron-formations(BF) has been discussedfor many years,as it has beendifficult to explain the accumulationof iron and silica in thesedepositsby chemicalprocessesalone.In this paper, we survey fte significanceof the presenceof microorganismsin microfossils and stromatolitesassociatedwittt BIF. The requirementsfor the growth of bacteriaare discussed.Microbially mediatedgeochemicalFocessesinvolved in the deposition of iron and sitca in thesesedimentsare considered.The influencethat microbial mats,hot springs,and deepseahydrothermal ventsmight haveon currentideasin geochemistryalsoareexamined.A recentlydiscoveredbiofrln *as able to sorb silica and presipitateircn both ashematiteandsideritein closeproximity; we suggestthat the microtrialreactionsoccurringin this biofikn could be similar to thosethat may haveplayed a part in the depositionof BIF. Biofilms createmicroenvirotrmentsthat allow the precipitation of minerals with distinctly different fields of stability, Since biomineralizationcan occur both by physico chemicalsorptionandby metabolicallyinducedreactions,suchreactionscould haveplayedan importantrole in the deposition of iron and silica in BIF and in metalliferoussedimentsfrom the early Archeanto the presentday. Keryords: bandediron-formations,biofilm, biomineralization,microbial reactions,microfossils,stromatolites. Somaanr Ir role desmicro-organismesdansla ddpositiondesformationsde fer rubann6esfait lbbjet de discussionsdepuisplusieurs ann6es,parce qu'il est difrcile d'expliquerI'accumulationde fer et de silice dans ces gisementsuniquementpar processus chimiques.Dans ce travail, nous dvaluonsI'importancede la prdsencede microorganismes dans les microfossileset les stromalolitssassosi6saux formationsde fer. Nous passonsen revtreles exigeancesdesbact6riesen croissance,ainsi que leur rdle dans les pocessus g6chimiques menante h ddpositiondu fer et de la silice dans les structuresgdologiques.Nous examinonsaussilinfluence qu'auraientpu avoir les coloniesmicrobiennes,les sourcesthermales,et les 6ventshydrothermaux sous-nrarins.Une biopellicule d€couverter&emment qui avait labilitd dabsorberla silice et de precipiter le fer sousforme dhdmatiteet de sid6rited"ns le mOmemilieu, nousfait trFnserque desr6actionsmicrobiennessemblablesauraientpu jouer un qui p€rmettent r6le important dansla ddpositiondesformationstle fer. De tels biopelliculescr€entdesmigro-environnements la pr6cipitation de mindraux ayant des champs de stabilitd nettement diffdrents. Comme il est possible d'assurcrune biomin€ralisationpar sorption physicochimiqueet par r6actionsiniti&s par mdtabolismed'organismes,de telles rdactions pourraientavoirjoud un r0le importantdansla d6positiondu fer et de la silice danr les formationsde fer et dansles s6diments m6tallifdrasdepuisI'arch6enpr6cocejusqu'i nosjours. (Iraduit par la Rddaction) Mots-cl6s:formationsde fer nrbann€es,biopellicule biomin#lisation, rdactionsmicrobiennes,microfossiles,stromatolites. t322 InrnoouctroN Speculationon the various processesthat produced the enormousconcentrationsof iron, silica and other metalsin bandediron-formations(BIF) has stimulated researchfor many years, for it has been difficult to explainhow suchvast amountsof iron and silica could have been concentratedin sedimenlsonotably during the Archean.Although there were various reports of the detectionof stromatolitesand microfossilsbv the tum of the century, it was not until Tyler's and Barghoorn'sdiscovery n 1954 of coccoid and filamentousmicrofossilsin the early hoterozoic Gunflint chert(-2.0 Ga old) that reportsof microfossilsin ironformations have proliferated in the literature. The potential role of microorganismsin the genesis of metalliferous sediments,puticularly in bandedironformations, now provides an incentive for further research. Bacterial activity has been demonstated (Mann L992) n the deposition of metals as well as in the weatheringand leachingofrocks. Ferris er al. (L987) andBeveridge(1989)alsohaveshownthat bacteriaare ableto accumulatemetalsfrom solutionby biosorption on a cell surface,as well as by active oxidative or reductive metabolism. A microbial biofilm (Brown et al. L994, Sawicki et al. 1995)recently discovered in an Underground ResearchLaboratory ((JRL) in ManitobaCBrownet al. 1989)hasshownthat iron from biotite in the granitic host-rock can be mobilized by microbial action. The iron is used as a source of energyby a microbial consortiumandthenprecipitated both in the oxidizedandreducedforms ashematiteand siderite, respectively. This biofilm provides new evidence for the role of biogenic processesin the deposition of metalliferous sediments,and since it preferentially accumulatessilica as well as iron, we suggestthat this type of microbial mediation could have beeninvolved in the depositionof bandedironformations. In this review, we examinethe history of researchon BIF, the requirementsof bacterialgrowth so the reader may be able to comprehendtle various microbially mediated mineral deposits occurring today, and the implications of these microbial reactions and their relationshipto the conceptsand models proposedfor the formation of both recentand ancientmetalliferous sediments. llsrony or MrcnosrAl Grocrcnrrsrny Assocr^rm wml BIF The suggestion that biological processesare importantin the depositionof iron-rich sedimentswas initially put forward by Ehrenberg (1836), but it was not until 1888that Winogradskywas ableto show that a bacterium,Izptothrix, is able to live and grow only where ferrous iron is presentin solution. These organismsglow a sheathsurroundingthe cells that is stainedbrown by accumulationof iron oxide. Since this coloration occurs only where living colls are present,Winogradsky(1888) proposedthat they must actively produce the ferric iron that becomes enmeshedin the sheath.He concluded,therefore,that oxidation of ferrous compoundsto fenic hydroxide is necessaryfor the growth of the organism. Since this processprovides energyfor cell growth, organic matter would not be required for energy production. However,Lieske(1911)proposedinsteadthat carbon derived from ferrous bicarbonatewould provide the necessaryenergy,and despiteWinogradsky'sfindings, the consensusuntil recently has been that organic matteris indeednecessaryfor cell growth. Since weathering of ordinary rocks should have continued on the same scale throughout the Precambrian and Phanerozoic.Van Hise & kith ( 19I 1) questionedwhetherthis couldbe the solesource of the iron and silica in BIF. Harder & Chamberlain (1915) suggestedthat, although the precipitation of ferric hydroxide from solution during the deposition of the Itabira (Brazil) iron-formation could have been purely chemical, it was more likely to have resulted from the operation of 'owell-known iron bacteria" (their term). Harder(1919)reviewedthe early ideason the relationship between iron-depositing bacteria and the geological environment.Gruner (1922) consideredit probablettrat both algae and hon bacteria contributed to the precipitation of organic colloids during the depositionof the Biwabik (Minnesota)ironformation. LaBergeet al. (1987)proposedthat the hecambrian iron minerals originated mainly as fine-grained, biologically precipitated ferric hydrates that later maturedto ferrihydrite and hematite.This ferric iron was then reducedby concomitantmicrobial degradation of organic matter to siderite, which later altered to magnetite. They suggestedfirther that in the sedimentary environment, ferric and ferrous iron minerals would have coexisted in metastable equilibrium. Current reviews of energymetabolismby Nealson & Myers (1990) and Lovley (1991) show that metabolic oxidation and reduction of inorganic ions, notably ofiron, by bacleriaaxenot only important but have a widespreadinfluence also upon the natural environment. If the sourceof ferrous iron had been the siagrant oceansbeneathan anoxic atmosphere,as proposedby Cloud & Licari (1968), this iron could have been convertedinto insolubleferric oxidesonly when there wasa changein the Precambrianahosphere dueto the evolution of oxidative photosynthesis(Cloud 1973, 1983).Major BIF would thereforebe found only within a shortinterval during the Early Proterozoic,beforethe atmospherebecamefully oxygenated. The highly metamorphosedIsua iron-formation in MICROBESAND BANDED IRON-FORMATIONS Greenlandis probablythe oldestknown BIF (3.8 Ga). It contains rounded carbonaceous,iron-coated microstructures(mainly oxides) that are more typical of organisms than of inorganic recrystallization @obbins 1987).The oldest definite microbial fossils yet describedare from the WarawoonaGroup (3.3 to 3.5 Ga) in WesternAustalia (Schopf& Packer1987), where the cells of filamentous aud colonial microfossils me preservedby the formation of stromatolites embeddedin carbonaceouscherts. Mcrocrystalline siderite and hematite in the Transvaal BIF (25 to 2.1 Ga) are considered to reflect the chemical environmentin the depositionalbasins,sincethe other mineralsappearto be eitherdiageneticor metamorphic in origin @eukes1983).James(1954)pointedout that the composition and sffucture of the precursor sedimentaryfaciesmust havebeenconfrolledby environmental factorsin the depositionalbasins,and that this would be reflected in the mineralogy and textural featuresof the lithofaciesderivedfrom them. Although major depositionof BIF was suggestedto have ceasedwhen eukaryoticphotosynthesisevolved sufftcientlyto producea stableoxygenatedatmosphere about 2.0 Ga ago (Cloud 1973),there are today many environments,smaller in extent,whereiron and silica arebeing depositedunderboth oxidizing and reducing conditions (Gross & Mcleod 1987, Rona & Scott 1993).Initially, the iron andsilica in BIF werethought to be derived exclusively from sedimentarysources, but now hydrothermalplumes are acknowledgedto 1323 havebeenthe main source(Gross1991,Isley 1995). The discovery in the late 1960s of hydrothermal ventsalong spreadingridgeson the seafloor(Jannasch & Wirsen 1981) and the investigationof surfacehot springs at Yellowstone @rock & Madigan 1991) provide partial analoguesfor the study of iron-rich metalliferoussediments.Modemhydrolithic sediments rich in iron, manganese,silica and sulfide minerals sunounding sites of hydrothermaldischargeprovide corroborationof the nature of the precursorsand the lithofaciesthat could havedevelopedftom them. In this review, we suggestthat microbial processes could have mediatedthe precipitation of iron, either oxidized or reduced,in narrowbandsinterlayeredwith beds of silica Microfossils and stromatolitesassociated with banded iron-formations indicate that prokaryotic organismswere presentby the t'me these sedimentswere being formed, althoughtheir specific role in the depositionof BIF hasyet to be determined. Rrqunmamrrs oF BAcIRTALGnowru Since microbial activity has such an impact on geologicalprocesses, it is importantto understandwhat these reactions might be. Microorganismshave the abilify to selectivelygathernutrientsinto the cell and to modily them so that they may serve either as cell building blocks or as an energysourcefor growth, the ofwhich has a considerableeffect on the consequence pH and Eh of the naturalenvironment. Frc. 1. Typical microfossil texture in magnetite- hematite - chert lithofacies in the Gunflint ircn-formation,ThunderBay, Ontario. t324 TTIE CANADIAN MINBRAIOGIST FIc. 2. Stromatolites,20 to 30 cm in diameter,from the Gunflint iron-formation,Thunder Bay, Ontario. It is difflcult to demonstate how microorganisms may have participatedin the deposition of iron-rich sediments,since the only evidencewe now have is their fossilized lemains, and it is not possible to determine from the cell morphology alone what misrobial reactionsmight have taken place. Evidense of microfossilsand stromatolitesin eady Precambrian BIF is relatively rare, and even where they were originally present,in many casesthey would havebeen desffoyed by later metamorphism.Figure 1 shows microfossils from the Gunflint iron-formation in Ontario,andFigure 2, a stromatolilefrom the Biwabik iron-formationin Minnesota. Microbes preferentially utilize the lightest isotope, so that an assessment of isotopedepletioncan provide further information on possiblemicrobial activity. fn somesediments,chemicalremnantssuchascarbonates and kerogen contain anomalously Light carbon, indicating that they were most likely formed tbrough biological activity (Winter & Knauth 1992). Microorganisms are usually visible only under the microscope. They are mainly unicellular and prokaryotic (without a separalenucleus), commonly consistingof a singlecell enclosedby a membranethat separates the metabolically active unit from the extemal medium. Eukaryotes, on the other hand, enclose their genetic material within a membranebound nucleus; some are unicellular, but most are multicellular organisiui. This group include the atgae and plants,as well as all of the alrimaltr1og6o-. Bacteri4 howeveq are the most important organisms that participatein chemicalinorganicreactionsin the natural environment;althoughthe basic metabolic pathwaysfor cellular growth and internal transfer of energyare similar in all organig6s,only bacteriashow such extraordinarydiversity in their ability to obtain energyfrom externalsources.Bacterialspeciesarealso versatilein their capacityto quickly produceenzymes (biological catalysts)to utilize any nutrient tiat may become available, 16os saaUing many extreme ecologicalnichesto be rapidly filled (bgaham et al. 1983). The availability of carbon substrates,energy sourcesandreducingpowsr in the naturalenvironment has furfluencedthe evolution of the energy reactions that bacteria are able to accomplish. Mauy geochemicalprocesses in naturalsyslemstakeplasewithin a wide rangeof pH, redox, and salinity, and theseare often detenninedfrom the result of reactionsof tle indigenous bacteria at water-rock interfaces @erris et al. 1987). Nutrients All life on Earttr is based on carbon. and this constitutes half of the bacterial cell mass. Other important elementsare oxygen, nitrogen, hydrogen, phosphorusand sulfir, together witl trace amounts of other elements, including iron. In the natural environmen! these elements are generally leached from ttre bedrock either by weatheringprocessesor microbial mediation. The requirementsfor cellular growtl are, tlerefore, the availability of these ngcessaryelements,a sourceofenergy, and a suitable habitat @rown 1994). In marine and terrestrial groundwatersowhere nutrientsare limited bacteriausually live in consortia within a biofilm or maq wherethe member$may also be symbiotic. The survival stategy of these asso- MCROBES AND BANDED IRON-FORMATIONS ciations is to adhereto a surfacein a film of organic material.Nufrientstendto concentrateat rock - biofitn - groundwater interfaces, where fluid movement continuallybrings new suppliesofnutrients to provide a richer food-source than that of the bulk fluid environment (Costerton et al. 1980. Sessile (sedentary)bacteria on these surfacesthus have an ecological advantageoyer those that are plar:ktonic (free-swimmingin the bulk fluid). In the natural environment today, biofilns are initiated by planktonic organismstlat colonize rock surfaces.Bacterial successionthen leads to a mature community,similar to that found in other ecosysterns. Exopolymeric substances,generally polysaccharides, are excretedby the bacteria, which accumulateand form a chargedlayer of slime surroundingthe consortia (Characklis & Marshall 1990). Utimately, owing to transfer limitations, the inner layer of a biofilm may become anoxic, stimulating the developmentof an anaerobicpopulation (Costertonet al.1994). Finally, ciliale prptozoawithin the biofilm may graze on the bacterialpopulationandthushelp to maintaina climax community(Locket al. 1984). Energy The major sourceof energyfor organismsliving on earthtoday is the sun.Solarenergyis utilized by plant photosynthesisto produceoxygenwhilst fixing carbon into organiccompounds(thathavereducingpotential). This carbon inco'rporatedas plant biomass is then utilized by animalsfor tleir growth. However, in the Archean,before oridative photosynthesishad evolved, and even today, in environments where neither sunlight nor biomass from solar energy can penetrate,primitive organisms (bacteria)must find other sourcesof energy.Sincethe maintenance of complex biological structures of the living cell is thermodynamicallyunfavorable,to sustainthemselvesand grow, organismsmust couple energy-producing oxidation-reduction reacfions to their endergonic biosyntletic ones. These redox reactionsare able to tansfer elecfronsfrom a donor (reducing potential), which becomesoxidized, to an acceptor,which is thenreduced. Oxygen is the most common elecfron donor to be utilized by living orggnis6s, but in environments where this is not available, such as the eady anoxic Earth, other donors are required. The sequenceof elecfron donorsinvolved in nature are, in descending order of thermodynamicallyavailableenergy:oxygen, nitrate and nifrite, N[ne, Fe], sulfate and carbon dioxide. The reduction of thesecompounds(electon acceptors) is generally coupled to the oxidation of organic matter (electon donor). This sequenceof bacteriallymediatedredox reactionsis the sameasthat found in the waler columns of lakes and sediments (Sfumm& Morgan1981). L325 Environment Bacteria play a major role in the control of the natural aqueousmilieu by their influence on the biological reactions of photosynthesis,respiration, and oxido-reductivechangesin the iron, sulfur and carbon systemsolargely determiningthe pH and Eh limits of the natural environment@aasBecking et al. 196O). Terrestial life requireswater in the liquid phase,thus the temperaturelimits for growth may range from below -5"C in Arctic seas to above 100oC (and possiblymuch higher) in deep-seathermalvents. When living organismsfirst arose approximately 4.0 Ga ago on this planet, tle atmosphere was reducing, so the early organisms evolved in the absence of oxygen. Early anaerobes would also have had to develop mechanismsto prevent being poisoned by oxygen radicals, the successful ones lscaming aerobes,and thosethat could not copewith oxygenpoisoningremaininganaerobic;as well, some bacteria (facultative) are able to live in either environment. Although filamentous bacteria -3.5 Ga old have been found that have fossil morphology similar to cyanobacleria@lue-greenprokaryotic algae) (Schopf & Packer 1987),it is almost certainthat stromatolites older than -25 Ga were composedof anoxygenic photohophs (purple and green bacteria) rather than oxygen-evolving cyanobacteria@rock & Madigan 1991). Recently, it has been reported @brenreich& Widdel 1994) that purple bacteriaare able to oxidize Fe2*to Fe* when this is coupledto the reduction of organic matter. Biological oxidation of iron would therefore have been possible before the evolution of oxidative photosynthesis,so that the formation of hecambrian stomatoliles would have been possible without the participation of oxygen-producing cyanobacteria(Castenholz1994). Eventually, as life evolved and became more complex,efficient oxidative photosynthesisdeveloped in eukaryoticalgaeandgreenplants,but beforeoxygen could have begun to accumulatein the atmosphere, the surface waters would first have had to become safurated. However, once the atmosphere did become oxic, eukaryotic and multicellular animals would have been able to proliferate (Woese 1994). Theseeukaryotesmay have grazedon the prokaryote communities,possiblyendingthe ageof stomatolites, since microbial mats cannot persist where tlere are efficient grazers(Castenholz1994). MtcnosIALMI.IRAL DEposrnoNToDAy There are various geological features being fashionedtoday by microbial mediation that can be relatedto ancientfossilizedforms. Descriptionsofthe biological involvement in several of these stuctures are describedbelow. 7326 THE CANADIAN MINERALOGIST both iron and silica are being deposited.Moreover, modern stromatolites are usually found only in Microbial matscontainlayersof different microbial carbonateenvironmenls"but the siliceousstomatolites communities;today, they generally consist of cyano- beingforrnedherearecomparableto thosefound in the bacteriain the uppermostlayer, various phototrophic Gunflint cherts. This similafiry supportsthe concept bacteriain deeperlayers until light becomeslimiting, that hot springs were a primary source of silica in and then degradingbacteria such as sulfate-reducers Precambrianiron-formations,and alsothat many early occupying the lowest and darkest layer @rock & fossil sfromatolitesmust havebeenbacterial,not algal Madigan 1991).Theseare dynamic systemso where in origin, sincealgaeonly evolvedlater ($Ialtet et al. photosynthesisthat occursin the surfacelayer of the L9s4). mat is balancedby decompositionat its base.Microbial mats are found in a variety of environments,notably Shallowseas thoseofvolcanic hot springsandshallowmarinebasins. Algal mats up to 30 cm thick have beendescribed Contemporaryhydrothermal sedimentsare being from Baja California (Horodyski 1977, Horodyski formedat severalplaceswithin the Santorinicaldera,in et aL L977).A variety ofmicroorganismscontributeto the eastern Mediterranean (Bostr0m & Widenfalk their formation, but their morphologyis conffolled by 1984). The sediments are largely authigenic iron filament abundance,flooding history, water depthand hydroxide,carbonate,and sulfide mineralsmixed with mostimportantly,by the degreeof desiccation.Several rock fragmentsand some clay. The topmost surface types of filamentous organisms contribute to the of the sediments,howeyer,consistsalrnostentirely of primary organic deposit, which is subsequently biogenic iron oxide-hydroxide formed on the stalls degradedand modified by further bacterial activity. of the bacteriumGalionellafemrginea (Holm 1987). If heavy rains flood these mat communities, the Owing to the proximity of the surface, there is depositionof larninatedsedimentceases,and instead, extensivedownwardadvectionof oxygen,which reacts up to 10 cm of siliceous sedimentmay be deposited with the vent hydrogensulfide to form sulfuric acid. over the surfaceof the mat (Stolz & Margulis 1984). This acid producesa local environmentquite different This new layer of sedimentis then recolonizedby a to that of the deepse4 andhencethe sedimentsalsoare different suite of organisms.Meanwhile,the siliceous dissimilar. sedimentsare reworked inlo an anaerobicmud that containsmetals,sulfur, and well-preservedsheathsof Deep-seafloorvents filamentou$and coccoidbacteria.An active microbial communitycanthusproducea largeamountof organic Metalliferous sedimentsaroundhydrothermalvents material which, althoughpreservedas a thin layer in in deepbasinsin the Red Seacontainfaciesof soft red the underlying mud, provides little other evidenceof to grey-brownbandedsedimentsthat are composedof the organisms that produced it Stolz & Margulis iron and base-metaloxides, hydroxides, sulfides, (1984)suggestedthat theserecentlaminatedsediments silicates and clay minerals @l Shazly 1990). These of Baja California bear a striking similarity to partially consolidatedsedimentsare generallymuddy, the laminalsd sedimentsand associatedcherts of the with micrometer-sizeparticles.The organismsfound ArcheanSwazilandSystem. associatedwith thesesedimentsare mainly planktonic foraminifer4 with only a few sulfate-reducingbacteria Hot sprtngs at the seawater interface, altlough isotopic data indicatethat pyrite wasbiologically formed. Sftomatolitesand algal mats are laminatedorgaooSedimentsdepositedaround deep seafloorthermal sedimentary structures that form through repeated ventsappearto provide a goodanalogyfor the studyof cycles of sediment accretionoin general reflecting BIF (Jannasch& Wirsen 1981, Jannasch& Taylor periodic intemrptions in their deposition. They are 1984).The submarinefood-chain.hereis basedon generally built at present by eukaryotic algae, but hydrogen sulfide, which chemosynthetic bacteria before eukaryotes evolved, prokaryotic organisms utilize to provide the primary sourceof food for the had formed similar organiccomplexes.Today,stroma- invertebratepopulation.The major sites of microbial tolites are being formed at Yellowstone both by activity are suspensionsof bacterial cells (Haymon eukaryotic algae and by prokaryotic bacteria. et al. 1993), biofilms gpwing on various surfaces hokaryotes preferentiallygrow where eukaryotesare (Tunnicliffe & Fontaine 1987) and filamentous unableto survive,usually when the conditionsare too microorganisms(Juniper& Fouquet 1988),as well as hot. Phylogenetic characterizationof the hot-spring symbiotic associations between chemoautotrophic sedimentsby moleculargeneticshasrecentlyrevealed prokaryotesand vent invertebrates.Most surfacesare a remarkablediversity of prokaryotic species@arnes coveredwith bacterial biofikns that contain iron-rich et ql. L994). Although Yellowstone waters generally encrustations.The biological productivity mound the haveonly a low concentrationof iron, in somegeysers vents is high compared to that of the Microbial mats MICROBESAND BANDED IRON-FORMATIONS L327 was irrigated by surface water used for mining activities (Brown et al. 1994).The water containeda range of microorganisms, and it had also been contaminatedwith blastingmaterialscontainingcarbon and nitogen, both essentialfor microbial growth. The biofilm grew over a period of several months to a thickness in places of 10 mm. Initially, it appeared grayrshwith light-brown sfreals, but orangemarkings developedlater. Runnels,formed within the biofilm by flowing water, were stainedblack internally. Lateq a white precipitateformed over theserunnels. Deposits of iron and silica (delectedby electron microscopy, X-ray diffraction and energy-dispersion spectroscopy)wererapidly forrnedon the bacterialcell walls and exfrapolymericslime @g. 4), althoughthe concentrationsof iron andsilica in the water werelow. Mdssbauerspectroscopy(Sawicki et al. 1995)showed that smallparticlesof protoferrihydritewereformedon the outer aerobic face of the biofilm" which later showedalterationto hematite.By contrast,at the inner anaerobicface of the biofilm next to the rock wall, ferrous iron was formed, which was then either Brornnarnou alr Uxpm.cnouxr RTSnARCH Leronaronv (JRL) sorbed direclly onto the biofilm i*elf, or reacted with carbonate from microbial fermentation to be The stimulusfor this paperwas our discoveryof a precipitated as siderite. The white precipitate was biofilm that was able to precipitateboth hematiteand found to be gypsum. Both siderite and gypsum are sideriteaswell asto adsorbsilica. This biofilm formed rarely found in this pluton. in the URL excavatedin the Lac du Bonnet granitic pluton of the CanadianShield (Brown et al. 1994, Mcnonru GSocHHvILSTRv Sawicki et al. L995).The excavationis naturally dry, The microbial reactionsthat cancausefhe formation with only two water-bearingfractures,but the biofilm (Frg. 3) was able to form on the surfaceof a lmge of differentmineralsin theseenvironmentswill now be boreholein the floor of a drift (4'2frm deep),whereit considered.Mobility of mineral ions in the geological surounding water, and dense swarms of shrimp feeding near the points of emissionindicate theseare optimal sites for the chemosyntheticgrowth of their filamentous misrobial epiflora (Wirsen et al. 1993). Tunnicliffe & Fontaine(1987)consideredthat although initial precipitationof the iron is bacteriallymediated, further deposition of metals is determined by the geochemicalconditionsof the ambientenvironment. Extensivedepositsof polymetallic sulfide andoxide sedimen8aroundvent sitesare formed by the transfer of geothermalenergyto microbial biomassby bacterial lithoautotrophy (growth on inorganic compounds). This fansfer ofenergy contributessignificantly to the large-scalegeochemicalprocessesof the oceanfloor, so that present-dayhydrothermalenvironmentscould be comparableto the processesthat occurredin the hecambrian seas.Baross & Hofinan (1985) further suggestedthat complexmicrobial ocean-floorcommunities in the Archean could have evolved relativelv rapidly aroundsuchactivehydrothermalvents. Ftc. 3. Biofilm formed in a boreholein the UndergroundResearchlaboratory, resulting from the precipitationof ferrihydrite, siderite,and gypsumin the slime layer. L328 TTIE CANADIAN MINERAI'GIST Ftc. 4. Thin section of the biofilm showing in sira biomineralization(arrows) around bacterialcells. environmentis influenced by the baclerial processes ferrous ions to form an initial precipitation of of sorption, accumulation, and precipitation. These amorphousferrous sulfide, altering later to pyrite. reactionsinclude dissimulatorymetabolismof various When these iron sulfide minerals are exposedat the compoundsas energy sources,active assimilation of surface,either by erosionor by mining, they can form metal ions into the cell, notably as metalloenz;rmeso the substratefor chemolithic sulfur-oxidizing microandpassivephysicochemicalaccumulation. organisms, notably Thiobacillus ferrooxidans The greatesteffect of microbial activity upon the (Jorgensen1983). These bacteria are able to derive environmentis tbrough dissimilatory metabolism(not suffrcient energy for gfowth from the oxidation of incorporatedinto ttre cell biomass),notably of iron pyrite. The optimal pH for this reactionis 2.0, whereas and manganeseas a sourceofbacterial energy.Since the internal pH of the cell is close to neutrality. This these metals do not have to enter the cell and can difference in pH provides a sufficient proton-motive be relatively ineffrcient, va$t amountsmay have to be force acrossthe cell membranethat iron and sulfur can altered to provide sufflcient energy for cell growth. be oxidized by the removal of electons. To maintain hon is the fourtl mostabundantelementon Earth.such electroneutality,thereis a concomitantinward flow of that it is readily available to provide an almost protonsthat are transforrnedinlo cell energywith the unlimiled inorganic sonrce of energy, albeit not a consumptionof oxygen (Cox & Brand 1984). In a particulady efficient one. Bacterial reactionsutilizing similar manner, manganesemay be oxidized by iron canhavea considerableeffect on the environmenl bacterial mediation and form manganesenodulesand by allering the pH and Eh, producing micronichesof concretions@hrlich 1963). different fields of stability that allow the deposition of various iron compoundsdependentupon the redox Reductionof ferric iron state. The dissimulatoryreductionof ferric to fenous iron, Oxidation of ferroas iron coupled to the oxidation of organic matter, is widespread in the natural environment (Lovley 1991). Pyrite is formed in sedimentary rocks by the Although an early study concluded that microbial bacterial reduction of sulfate (generally from marine reductionof ferric iron was non-enzymatic(Starkey& waters)to hydrogensulfide; this reactschemicallywith Halvorson Dn), it has since proved impossible to MICROBESAND BANDM IRON-FORMATIONS demonstratethat ferric iron canindeedbe reducednonenzrymatically.In fact, it has beenconsistentlyshown that ferric iron in microbial culturesis only reducedas a result of direct enzymaticaction (Lovley 1991). The organisms responsible for the enzymatic reduction of ferric iron have only recently been isolated,althoughthey havebeenknown for morethan a century(Winogradsky1888).Geochemicalevidence indicates il1a1fissimilafqry respiratory reduction of ferric iron may have evolvedprior to other respiratory processes,such as the reduction of sulfate or nitrate (Walker 1984). Since ferric iron reducersare able to outcompeteboth sulfate-reducersand methanogens (reducers of carbon dioxide) as electron acceptors (Stumm& Morgan 1981),this reactionis the one that will preferentiallyoccur in nature.Thesebacteriahave beenidentified in sediments,suggestingthat they could have also been responsiblefor late post-depositional reductionof ferric iron (Lovley et al. 1990).The iron reactionszuerunongthe most important geochemical processesin anaerobic sedimentary environmentso since they can releasethe highly insoluble ferric iron from the rock massinto the groundwaterby reducingit to the more solubleferrousstate. Until recently, all black iron precipitatesin natural environments were consideredto be iron sulfrdes. mainly pyrite as described above. However, it has now beenfound that sincebacterialreductionof ferric iron is energetically preferred to the reduction of sulfate, ferous iron is producedrather than sulfide. The ferrousiron thenreactswith dissolvedcarbonateto form siderite (Colemanet al. 1993,Roden & Lovley 1993). The formation of siderite has also been demonstratedin the biofilm from the URL @rown et al. L994,Sawicki et al. 1995). Magnetiteformation Many bacterialen4nnesrequire a metal to conduct catalysis;theseare usually fransition metalsthat have several oxidation stales in the natural environment (Wackettet aI. 1989).The metalsare assimilatedinto the cell by specifiic transport-systems,allowing the bacteria to collect the metals from an environment where they may be presentin only minute amounts. Some bacteria contain chains of magnetosomes (magnetitecrystals),which make them magnetotactic and causethe cells to become orienled in the geomagneticfield @rock & Madigan 1991).However,the amountof magnetiteincorporatedinto thesebacteriais minuscule in comparison to that formed by the dissimilatory energy-producingreactions. Studies of anaerobicsedimentssuggestthat bacteria are able to producelarge quantitiesof ultafine-grained magnetite whenreductionof ferric iron is coupledto oxidationof organic matler (Lovley et al. L987). This processis likely to have caused the accumulation of large amountsof magnetitein iron-formations,presumably t329 under conditions that are more oxidlzing than where sideriteis formed. Examinationof modern depositsand experimental synthesessuggestthat ironstonesare forrned by the gels @nhig et al. crystallization of Si-Fe-O{H 1992),which occur as a result of hydrothermalfluids mixing with seawater.Since it is unlikely that tlere would have been a sufficient period of time for significant quantitiesof iron to be precipitated,other factors,suchasiron-oxidizing bacteriaableto facilitate low-temperatureprecipitationof ferric iron, may well havebeeninvolved. Sorption: the cell as a polyionic trap Passivephysiochemicalbiosorption is the type of microbial mediationthat occursbetweeninorganicions and microbial cellular components,whether dead or alive. Many bacteriaproduce an outennostenvelope of slime that servesas a buffer betweenthe cell and the external environment. which has unsatisfied chargesthat promote a polyionic trap for ionic and electrostaticbinding ofmetals and silicates(Geesey& Jang 1990). Bacterial cells are efficient in forming metallic silicatesandfine-grainedminerals,sincethese reactionsreducefhe level of toxic metalsin solution. Silicate binding to Bacillus subtilis has been demonsftated(Umrtia & Beveridge1993),in a casein which the depositionof silicate is dependenton the elecffopositive charge of the cell. The formation of fine-grainedmineralsalso occursin the S-layer(slime) a cyanobacteriumfound in freshof Synechococcus, water lakes (Schultze-Lam& Beveridge1994).In this caseomin916l formation begins as the deposition of minute crystals of glpsum, but as the pH of the microenvhonmentis increasedby metabolic activity, the precipitatechangesto calcite.Active cells can shed the mineralizedS-layer,but as they age they become entombed.andform calcitebioherms. Epilithic microbial communitiesfound ubiquitously on submergedrosksarshighly mineralized(Konhauser et al. 1994), and the biofilns, regardlessof their substratum lithology, consistently form iron and aluminum silicates, indicating that biomineralization is a surface process associated with the anionic nature of the cell wall. These biofilms seem to dominate the rock-water interface and to determine which minerals will ultimately become part of the riverbed sediment. Sitca is one of the major componentsof BIF, but any microbially mediatedsystemfor silica deposition posesa problem,sincesilica-metabolizingprokaryotes are unknown, and eukaryotes only evolved later. Thereforeomediation by bacteria of the precipitation of silica in Archean iron-rich banded sediments would have had to be by passive physiochemical sorptionsuchas describedabove,ratherthan by active metabolism. 1330 THE CANADIAN MINERALOGIST Btournrr.elze.noN MopsIFoRrrrE Gmwsn or BIF Microorganismshavebeenpresenton Earthfor 907o of its history, and so it is to be expectedthat they shouldhaveplayeda fundamentalrole in the evolution ofour naturalenvironment.Significantalterationofthe biosphereby microorganismsis causedby their needto obtain nutrients and energy for growth. One of the major effects of this requirement is the change in valency in the caseofinorganic ions that are utilized by bacteriaas a sourceof energy;this is reflected in the modification of pH and Eh, thus altering the solubilities of the dissolvedions. Organic life may leave its signature in the sediments, and evidence of organic remains have been found in BIF and the associatedblack shales.In many cases, the carbon is isotopically light, indicating microbial activity; this also can be correlatedwith an increasein the concentation of iron (Walker 1984). Sfromatolites are fossilized microbial mats that contain entrappedsediment between layen of filamentous organisms.Although silica is not directly metabolizedby prokaryotes,it can be precipitatedby physicochemicalreactions with the microbial slime layer or cell wall. Modern $tromatolitesare usually carbonaceous,not siliceous, and contain oxygenproducingorganisms,but in appropriateenvironments, suchasYellowstoneaudBaja Califomi4 stromatolites are today being formed that contain prokaryotic organismsin a siliceous matrix. These sfiomatolites have a similar morphology to those of the Archean, suggestingthat they could havebeenformedby similar means. Microorganisms require a source of energy for growth, but this doesnot necessarilyhave.to be light from tle sun. Metalliferous sediments presently forming at the deep-seavents utilize chemolithotrophic, not photosyntletic, energy. Furthermore, bacterial photosynthesis did not initially produce oxygen; it was only later when cyanobacteriaevolved that oxygen was directly generated,but it would still have been limited in amount and rapidly utilized. Oxygen could only have accumulated in the amosphere when the water became saturated,after eukaryotic algae and greenplants evolved in the late Proterozoic. Ho'ffever,oxidationof ferrousiron probablywasthe earliest photosyntheticabiJity evolved by primitive organisms (Ehrenreich & Widdel 1994), which suggeststhat free oxygen would have been unnecessaryfor the deporl6oasf 6xidizediron beds.Microbial organismsin shallow seasduring the Archean would have received unrestrictedlight from the sun, which they couldhaveutilized to lay down thin layersofironrich matsover large lateral areas.Episodic or seasonal flooding of thesemats may have coveredthem with siliceous sediments.which would ttren have been recolonizedby photosyntheticbacteriaoncethe water retreated.The questionis not, therefore,whether the atmosphere contained sufficient oxygen for the deposition of oxidized iron, but rather, whether precipitation of large quantities of ferric iron could have occurredby microbial mediationin the aqueous depositionalenvironmentof that time. To judge from the BIF that we know today,this whole processwould havehad to be repeatedmany times over the millennia to allow suchnumerousbedsto accumulate. Many BIF contain thin bands of silica alternating yiX[ millimeter-thick bands of minerals containing ferrous or ferric iron (or both). It has beenditftcult to explain how chemical processesalone could have producedtheseresults. Our recent study of the URL microbial biofilm does offer an explanation,since it showsthat microbial consortiaare capableof forming different microenvironments(stability fields) within a biofikn, thus allowing precipitation of both oxidized iron as ferrihydrite and reducediron as siderite.This microbial mediation permits two very dissimilar iron minerals to be precipitatedin close proximity. Both oxidized and reducedstatesof iron are found in BIF, but the statein which they were originally precipitated would have been detenninedby the oxygen potential (possibility of metabolic microbial oxidation) in the environmentat the time of deposition.Since iron can be precipitated in both oxidized and reduced forrns by bacterial mediation, it is no longer necessary to postulatelater metamorphicalteration in order to explain the stateof the iron in BIF. Stomatolites at Yellowstoneand the biofilm in the URL show that iron, evenin very low concentations, may be precipitatedby microbial actionfrom solution. Although the present ocean environments do not provide large areasofiron-rich shallow watersunder an anaerobicafuosphere,suchaswererequiredfor the massive Archean and Proterozoic BIF, there are metalliferous sedimentsbeing depositedtoday under comparableenvilonments,but in smallerareasaround hot springsand hydrothermalvents (Gross& Mcleod 1987). Coxcr-usroNs The microbial precipitationof iron and silica in BIF would have dependedupon the natural environment at the time of deposition. Silica could have been accumulated by physicochemical sorption on the microbial biomass, whereasiron would more likely have been metabolically utilized by the bacteriaas a sourceof energythat could havebeendepositedeither in an oxidized or reducedstate, dependentupon the prevailing pH and Eh. In the absenceof oxygen,iron would have beenprecipitatedin the reducedform as sideriteor iron silicate,or possiblyaspyrite in a marine environmenl Where oxidizing potentialwas available, the iron would more likely have beenprecipitatedas MICROBES AND BANDED IRON-FORMATIONS r331 fenihydrite or magnetite, possibly altering later to BRowN,D.A. (1994): The effects of bacteriaon crystalline rock In Scientific Basis for Nuclear WasteManagement hematite.Microbial mediation appearsto be essential X\ru (A. Barkatt & R.A. Van Konynenburg,eds.).Proc. for the deposition of naxrow interbeddedlayers of Maerialx Res..Soa 333. 663-679. minerals rich in iron and silica found in the typical oxide, silicate, and carbonateBIF lithofacies. The Kauws.n, D.C., Sewrcrr, J.A. & Bs\rRDcE, T.J. (1994): Minerals associatedwith biofilms occurring on mineral bands appear to be discrete and to have exposed rock in a granitic Underground Research maintainedttreir chemical composition and integrity l-aboratary.Appl. Environ.Microbiol.ffi , 3182-3191'. throughoutsubsequentdiagenesisand metamorphism. Althoughit is extremelydifficult to unravelthe genesis CAsrENHotz,R.W. (1994):Microbial matresearch:the recent of PrecambrianBIF, our presentunderstandingof the past and new perspectives./z Microbial Mats (L.J. Stal relevantmicrobial reactions,takenin conjunctionwith & P. Caumette,eds.). Springer-Verlag,Berlin, Germany investigationsof modernanaloguesof BIF, show that (3-r8). most if not all, of thesemetalliferoussedimentscould only have been accumulated through microbial Cnenacrc-rs,W.G. & MARSITAII,K.C. (1990):Biofilms. John Wiley & Sons,New York, N.Y. mediation. Acro,IowLDcHvm,ns The commenls of Richard Sparling and Barbara Sherriff, togetherwith thoseof severalreviewersand editors,aremost gralefirlly acknowledgedfor the great improvementthey havemadeto the presentationof our ideas. Ct oup, P. (1973):Paleoecologicalsipificance of the banded iron-fonnation.Econ,Geol,68. 1135-1143. (1983): Banded iron-formation - a gradualist's dilemma- /n hon-Formation: Facts and hoblems (A.F. Trendall & R.C. Monis, eds.).Elsevier,Amsterdaru The Netherlands(401416). & LIcanr, G.R. (1968): Microbiotas of the banded iron formations.Proc, U,S.Nat.Acad. !ci.61,779-786, RErmeNCFs Cor.eMAN, M.L., Hmrucr, D.B., l,ovmv, D.R., WHnE, D.C. K. (1993): Reductionof Fe(ff) in sedimentsby & PyE, BAAsBEcrqNG, L.G.M.,Kapralv,LR. & MooR4D. (1960): bacteia. Nature 36.l, 43G538, sulphate-reducing Limits of the naturalenvironment in termsof pH and potentials. oxidation-reduction "LGeol.6, 243-284. DgBER, D., CAtDwHr, CosrmroN, J.W., LewANDo$/sxx,2., BARNES, S,M.,Furuyce"R.E.,Jrprnms,M.W.& PACE, N.R. (1994):Remarkablearchaealdiversity detectedin a Yellowstone NationalParkhotspringenvironmenl Proc. U.S.Nat.Acad.Sci.91,1609-1613. D., KoRBER,D. & JauEs, G. (1994): Biefilms, the -2142.' customizedmicroniche.J. BaoertoL 176. 21,37 NrcrEL, J.C. & Leoo, T.L (1986): Suitable methods for the comparative sfirdy of free-living and surface-associated bactorial populations. /n Bacteria in Nature (J.S.Poindexter& E.R. Leadbetter,eds.).Plenum Press,New York, N.Y. (49-84). BARoss,J.A. & Hornraer.rN, S.E. (1985): Submarine gradientenvironments hydrothermal ventsandassociated assitesfor theoriginandevolutionof.ltfe.Origin*Life 15, 3n345. Cox, J.C. & BRAND,M.D. (1984): kon oxidation and energy conservationin the chemautotrophThiabadllus Bwxrs, N.J. (1983):Palaeoenvironmetal settingof ironferrooxidans. /r Microbial Chemoautotrophy (W.R. formationsin the depositional basinof the Transvaal Strobl & O.H. Tuovinen, eds.). Ohio State University supergroup,SouthAfrica .ln kon-Formation Factsand hess, Columbus,Ohio (31-46). hoblems(A.F.Trendall& R.C.Morris,eds.).Elsevier, (13l-210). Amsterdam, TheNetherlands Durtrc, N.C., Srore, J., DAvDsoN, G.J. & LancE, R.R. BEVERDcE,T.J. (1989): Metal ions and bacteria-/n Metal Ions and Bacteria (T.J. Beveridge & R.J. Doyle, eds.1. JohnWiley & Sons,New York N.Y. (1-29). Bo$ROM,K. &Wnmwer,r, L. (1984):The origin of iron-rich muds at the Kameni Islands, Santorini, Greexe,Chem Geo|.42,203-218. BRocK, T.D. & MADIcAN, M.T. (1991): BiologX of Microorganisms (6th ed.). Prentice Hall, Englewood Cliffs, New Jersey. (1992):Cambrianmicrobial andsilica gel texturesin silica iron exhalites from the Mount Windsor volcanic bel! Australia their petrography,chemistry,al.d oig1n. Econ, Geol.82"7&-7U. EnRE{BERc,D.C.G. (1836): Vorldufige Mttheilungen iiber das wirkliche Vorkommen fossiler Infusorien und ihre grosseVerbreitung.Annalen dcr Plrysik und Chemie38, 2B-2n. A. & WDDH.,F. (1994):Anaerobicoxidationof EnRg.{RECrr, ferrous iron by purple bacteria a new type of photrophic metabolism.AppL Environ Microbiol. 60, 45174526. BRowN,A., SooNAwAra,N.A., Evmrrr, R.A. & Kevwqv, D.C. (1989):Geologyandgeophysicsofthe Underground Emucn, H.L. (1963): Bacteriology of manganesenodules. Research Laboratory site, Lac du Bonnet Batholith, l. Bacterial action on manganesein nodule enrichments. Manitoba.Can.J. Eanh Sci.26. 404 425. Appl. Microbiol. 11, 15-19. t332 TIIE CANADIAN MINERALOGIST EL SHAay, E.M. (1990):Redseadeposits./n Ancient Banded kon Formations @egional Presentations).Theophrastus Publ. S.A., Athens,Greece(157-222). & Wruru, C.O. (1981):Morpholggicalsurveyof microbial mats near deep-sea thermal yents. AppL Environ Microbiol. 41, 528-538. FERRS, R.G.,FrFE,W.S. & BwmDcB, T.J. (1987):Bacteria JoRcB{sE{,B.B. (1983): Morphological survey of microbial as nucleation sites for authigenic minerals in a metalmats near deep-sea thermal vents. AppI. Environ. contaminatedlake sediment.Chem,Geol. 63, 225-232. Mturobiol.4l.528-538. Grnssy, G.G. & Jarc, L. (1990): Extracellularpolymersfor metal binding. In Microbial Mineral Recovery (H.L. Ehrlich & C.L. Brierley, eds.). McGraw-I{ill Publ. Co., New York, N.Y. Q23-247). Gnoss,G.A. (1991): Geneticconceptsfor iron-formationand associatedmetalliferoussediments.Econ Geol.,Monogr. 6,51-81. & McLEoD,C.R. (1987): Metallic mineralson the deepseabed.Geol. Surv. Can.,Pap,E6.2l, Gnuxen, J,W. (1922): The origin of sedimentary ironformations: the Biwabik formation of the Mesabi ranse. Econ.GeoI.17.N746A. Hanom, E.C. (1919): Iron-depositing bacteria and their geologicrelations.U.S.GeoLSurv.,Prof. Pap, ll3. & CHaTIrRLAN, R.T. (1915): Geology of central MinasGerais,Brazil.J. Geol.?3,341-378. Ilewor, R.M., FonNem,DJ., Vor.r Da[[{, K.L., LtrrBy, M.D., PERFn,M.R., Eorr,roxp, J.M., SuNrs, W.C., m, Lutz, R.A., GRBlv'm, J.M., CARBorrE,A.,WRrcIIr, D., Mcl,AUGItrB.r,E., SlvtrrH,M., Bmue, N. & OrsoN, E. (1993): Volcanic eruption of the mid-oceanridge along the East Pacific Rise crest at 9o45'-52'N: direct submersibleobservationsof seafloor phenomenaassociatedwith an eruptioneventin April, L99I. Eanh Planet. Sci.Lett.119,85-101. HoLN4,N.G. (1987):Biogenic influenceson the geochernistry of certain femrginous sedimentsof hydrothermalorigin. Chem.Geol. 63,45-57. HoRoDYSKI, R.J. (1977):Lyngbyamats aJlaguna Mormona, Baja California, Mexico: comparison with Proterozoic stomatolites.J. Sed.Petrol. 4:1.1,305-1,320. -.=-_ BroBsER,B. & HAA& S.V. (1977):laminated algal mats from a coastal lagoon, Laguna Mormon4 Baja Califomia" Mexico. J. Sed Petrol. {1, 68A-696. Incnanau, J.L., Meet,oe, O. & Nmsanm, F.C. (1983): Growth of the Bacterial CelL Sinauer Associates,Inc., Sunderland.Massachusetts. IsLiEY,A.E. (1995):Hydrothermalplumesand the delivery of iron to bandediron formation.J. Geol. 103,169-185. Jarurs, H.L. (1954): Sedimentaryfacies of iron-formation. F.con.GeoI. 49, 235-293. JANNAScH,H.W. & TAyLoR, C.D. (1984): Deep-sea microbiology.Ann Rev.Microbi.ol, 3E, 487-514. Jwpm., S.K. & Fouqusr, Y. (1988):Filamentousiron-sifica deposits from modern and ancient hydrothermal sites. Can Mtupral. 2,6,859-869. KoNnAUsR, K.o., scEt[Ta-LAM, S., Fhrus, F.G., Fvrs, W.S., Loxcsrarrr, F.J. & Brvenoce, T.J. (1994): Mineral precipitation by epilithic biofiLns in the Speed River, Ontario, Canada"Appl. Environ. Microbiol.60, 549-553. I.eBm.cs, c.L., RoBBn{s,E.I. & HAN,T.-M. (1987):A model for the biological precipitation of Precambrian iron formations. A. Geological evidence. 1z Precambrian [email protected]. Appel & G.L. LaBerge, eds.). TheophrastusPubl. S.A., Athens,&we (331-342). Drsrs, R. (191l): Beitragezur Kenntnisder Physiologievon Spirophyllarn ferragineum Ellis, ernem typischetr wiss.Bot. 49,9l-lX, Eisenbakterien.,/alrb. Loc& M.A., War,t,ecB,R.R., CosrmroN, J.W., Vwrulo, R.M. & CHARLToN, S.E.(1984).River epilithon: toward a structural-functionalmodel. OIKOS42, 10-22. LovLiEy, D.R. (1991): Dissimilatory FeOrD and Mn(IV) redtctton. Microbiol, Rev. 55.259-287. Cuarrue, F.H. & Pnnt,rps,E.J.P.(1990):FeOIDreducing bacteria in deeply buried sedimens of tle Atlantic CoastalPlain. Geolngy18, 95+957. Srorz, J.F., Nono, G.L., Jn. & Pm;.ps, EJ.P. (1987): Anaerobicproduction of magnetiteby dissimilatory iron-reducingmicroorganism.Nanre 330, 252-254, MANN,S. (1992):Bacteiaandthe Midas tawh. Narure357, 358-360. NaarsoN, K"H. & MyRs, C.R. (1990): hon reduction by bacteria: a potential role in the genesisof bandediron formations.Arz. J, Sci.290-4, 3545. RoBBD.IS, E.I. (1987):Appelellafenifera, a possiblenew ironcoated microfossil in the Isua iron-formation, southwestern Greenland. /n Precambrian Iron-Formations (R.W.U. Appel & G.L. IaBerge, eds.). Theopbrastus Publ. S.A., Athens,Greece(l4l-154). RoDB{, E.E. & Lovr.sv, D.R. (1993): Dissimilatory FeOrD reductionby the marine microorganismDesulfuromonas acetoidans, Appl, Environ Microbiol. 59, 73+7 42. RoNa,P.A. & Scorr, S.D. (1993):A specialissueon seafloor hydrothermal mineralization: new perspectives. Econ.Geol.88. 1935-1975. MICROBESAND BANDED IRON.FORMATIONS SAwrcK, J.A., BRowN,D.A. & BsvRDcE, T.J. (1995): Mcrobial precipitationof sideriteand protoferrihydritein a biofilrn. Can^Mineral.33, l-6. ScHopF,J.W. & PAcKER,B.M. (1987): Early Archean (3.3-billion to 3.5-billion-year-old) mioofossils from WarrawoonaGroup,Australia.Science237, 70-73. ScHuLra-LAM, S. & BEvERIDcE,T.J. (1994): Physicochemical characteristicsof the mineral-forming S-layer from the cyanobacteriumSynechocuccusstrain GLZ. Can.J. Microbial. 40, 216-223. Srenrrv, R.L. & HALvoRsoN,H.O. (1927): Studieson the transformationof iron in naf,re. Soil. Sci,U.38L402, 7333 VAN IIIsq C.R. & IffrH, C.K. (1911): Geology of the Iake Superiorregion. U,S.GeoLSurv.,Morngr. 52. W.H. & WABH, C.T. WAcKErr, L.P., OnMs-JoHNsoN, (1989):Transitionmetalenzymesin bacterialmetabolism. InMetal lons and Bacteria(T.J. Beveridge& R.J. Doyle, eds.).JohnWiley and Sons,New Yorh N.Y. (165-206). Wer,r<m"J.C.G. (1984): Suboxic diagenesisin bandediron formations.rVarure 3n9, 3dt0-342. Walrm, M.R., Bauro, J. & Bnoc6 T.D. (1954):Siliceous algal and bacterial strodatolites in hot spring and geyser effluents of Yellowstone National Patk Science 178, 402405. Srorz, J.F. & Mencu,rs, L. (1984): The stratified rnicrobial WnrocRADsKy,S. (1888): Ueber Eisenbacterien,Botanischc z. M.261-270. communityat Iaguna Figueroa,Baja Califomia Mexico: laminatedmicrobial a possiblemodel for PrePhanerozoic communitiespreservedin chert..InOrigins of Life 14 (J.P. WINTB, B.L. & Knetmr, L.P. (1992): Stable isotope geochemisnryof cherts and carbonatesfrom the 2.0 Ga Fenis, ed.).Reidel Publ. Co., Dordrecht,The Netherlands (671-679). Gunflint Iron Formation:implicationsfor the depositional setting,and'the effects of diagenesisand metamorphism. Precainb. Res.59, 283-313. Sruw, W. & Moncex, J.J. (L981):Aqaatic Chemistry.Iohn Wiley & Sons,New York, N.Y. Wnsuw,C.O.,Jelwascr, H.W. & Molvwreux, AJ. (1993)l Chemosyntdeticmicrobial activiry at Mid-Atlantic Ridge TtrNMcI-itrFE, V..& FoNrAiNE,A.R. (1987): Faunal compohydrothermalvent sitrs. I. Geoplrys.Res.9E; 9693-9703. sition and organic surfaceencrustationsat hydrothermal vents on the southernJuan de Fuca Ridge. J. Geophys, WoEsE,C.R. (1994): Microbiology in transition, Proc. Nat. Res.92,11303-1 1314. Acad. Sci.USA 91. 1601-1603. TyLm., S.A. & Baneroorut, E.S. (1954): Occurrenceof structurallypreservedplants in Precambrianrocks of the CanadianShield.Science119, 60G608. URRUTA,M.M. & Bevmoce, T.L (1993): Mechanismsof silicate binding to the bacterial cell rvall n Badllus subtilis. J. BaoerioL 175, 193G1945. ReceivedDecem.ber5, 1994, revised.manuscript accepted August8, 1995.