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Research in Microbiology 154 (2003) 611–617www.elsevier.com/locate/resmi

Mini-review

Archean microfossils: a reappraisal of early life on Earth

Wladyslaw Altermanna, Józef Kazmierczakb,∗

a Centre Biophysique Moleculaire (Exobiologie), CNRS, Rue Charles-Sadron, 45071 Orléans, Franceb Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, 00818 Warszawa, Poland

Received 30 July 2003; accepted 20 August 2003

First published online 21 August 2003

Abstract

The oldest fossils found thus far on Earth are c. 3.49- and 3.46-billion-year-old filamentous and coccoidal microbial remains in roPilbara craton, Western Australia, and c. 3.4-billion-year-old rocks from the Barberton region, South Africa. Their biogenicity wasquestioned and they were reinterpreted as contaminants, mineral artefacts or inorganic carbon aggregates. Morphological, geocisotopic data imply, however, that life was relatively widespread and advanced in the Archean, between 3.5 and 2.5 billion ywith metabolic pathways analogous to those of recent prokaryotic organisms, including cyanobacteria, and probably even eukaryterminal Archean. 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved.

Keywords:Archean; Early life; Microfossils; Stromatolites

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1. Introduction

The time period and the environment surroundingappearance of the oldest fossils on Earth provide imporinsights into the origins of life. The Precambrian Eahistory, from the beginning of our planet c. 4.56 billioyears ago (Ga= Giga annum) to c. 0.545 Ga, when tfirst skeletal shelly fauna appeared, is divided into the oArchean lasting until 2.5 Ga and the younger, subseqProterozoic. When carrying out research on the origin ofPrecambrian palaeontology serves as a test for theoreconsiderations and experimental data, and helps to aour understanding of evolutionary pathways and molecclocks. With a boost in the general interest in exobiolo(astrobiology), a discipline yet barren of a true study objthe understanding of early life on Earth, and particularlyArchean microfossils, also becomes increasingly imporfor exploring the possibility of extraterrestrial life.

Three main lines of evidence in the search for eaArchean life exist: Chemical evidence (carbon-isotopicbiomarker detection), morphological evidence (microsco

* Corresponding author.E-mail address:jkaz@twarda.pan.pl (J. Kazmierczak).

0923-2508/$ – see front matter 2003 Éditions scientifiques et médicales Eldoi:10.1016/j.resmic.2003.08.006

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detection of microfossils) and biosedimentological interptation of structures like stromatolites.

Chemical evidence of carbon isotopes (RuBisCO-tfixation of12C in higher proportions than13C) reported fromArchean rocks of Greenland suggests that life existedEarth as early as 3.8 billions years ago [11,20,25,26]. Threports of ancient life, however, were repeatedly criticisedetection of traces of later rock colonialisation by contanating (endolithic) bacteria, or as not in agreement withresults of detailed mapping and geological interpretatiorock formations (i.e., the rocks are younger than 3.8 billyears) [21,36,42].

The earliest microscopically recognisable microfoswere reported from the 3.49 Ga Dresser Formation [35]from the 3.46 Ga Apex Chert of the Pilbara craton, AustraFrom the Apex sedimentary rocks, eleven taxa of cellulapreserved filamentous microbes were described [28]. Restudies, however, have questioned the validity of some oEarth’s oldest fossils from the 3.5 to 3.4 Ga rocks of SoAfrica and Australia, implying that the structures mimickibacterial fossils may be contaminants, fluid inclusions [1or carbon threads formed abiologically in hydrothermenvironments [6]. The controversy and the public debatethese findings have attracted much attention in the sciencommunity [9,10,15]. Any report of the record of ea

sevier SAS. All rights reserved.

612 W. Altermann, J. Kazmierczak / Research in Microbiology 154 (2003) 611–617

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The earliest assured cyanobacterial microfossils wereported from Neoarchean rocks (2.7–2.5 Ga). The earcyanobacterially/bacterially mediated biomineralisation wreported from 2.6 Ga carbonate rocks [4,14,17,19]. Fthermore, the startling findings of biomarkers like methhopanes and steranes [7] in the 2.7 Ga shales of the ForteGroup, Pilbara Craton, Western Australia indicate oxygephotosynthesis, and the existence of eukaryotes alreathe Neoarchean. Hence the metabolism of the Neoarcbiota was essentially similar to that of modern organisand included anaerobic fermentation, anoxygenic phsynthesis, oxygen-producing photosynthesis, and aerrespiration in autotrophs and heterotrophs. These dataconsistent with estimations of minimal divergence timesthe major bacterial and archaeal phyla [33].

2. Identification of the problem

Although several decades have passed since thedescription of Archean microfossils, the palaeontologrecord of the Archean is disappointingly scanty, accounonly for about 30 accepted taxonomic occurrences. Archrocks, although rather widespread in old cratonic coresusually strongly altered, often beyond recognition of thprimary structure and composition, by geological procesof denudation, low temperature recrystallization (and weering diagenesis), tectonism (including plate tectonics),thermal and pressure alteration (metamorphism). Imceptibly metamorphosed rocks, particularly from the eaArchean (>3.0 Ga), are extremely rare and occur mainlythe Kaapvaal craton of South Africa (Barberton greenstbelt) and on the Pilbara craton of Western Australia.known rocks older than 3.5 Ga are severely metamorphoincluding those of the Isua greenstone belt of Greenlaand underwent metamorphism and tectonism underperatures reaching 600◦C and high pressure (>5 kbar).Under such conditions new minerals form in the rockspossible organic content alters to graphite and amendisotopic biosignature [36]. Nonetheless, morphological, gchemical and isotopic data from rocks 3.5 Ga and younimply that Archean life forms were widespread and ratively advanced, having entered metabolic pathwaysserve analogous organisms today.

The clearest macroscopic witnesses of Archean lifestromatolites occupying and building carbonate platfoand reef-type bioherms (limestone, CaCO3 and dolomite,CaMgCO3 or chert rocks, SiO2). Stromatolites are defineas lithified biosedimentary structures, growing throughcretion of laminae by the entrapment of sediment anby direct precipitation of carbonate, as the result of thetivity of microbial organisms [40]. Other definitions alsinclude possible and pure chemical precipitates [12]. Inlatter case, stromatolites, of course, do not necessarily

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Fig. 1. (A) Late Archean digitate microstromatolitic structures (KogelbFm., Kathu borehole, South Africa) composed of silicified, darkerlighter calcium carbonate laminae. (B) Almost identical modern calcous microstromatolitic structure from quasi-marine crater Lake Moton Satonda Island (central Indonesia) composed of similarly alternalighter and darker laminae originating from in vivo (darker calcitic laminand early post mortem (lighter aragonitic laminae) calcification of cocccyanobacteria. Cyanobacterial capsules are occasionally excellentlyserved due to early diagenetic silicification. (Thin section micrographtransmitted light.)

idence life. Stromatolite researchers are thus divideddifferent groups, those who follow the biological approato stromatolites and others who treat stromatolites rathesedimentary or biosedimentary structures. Naturally, thgroups also differ in their opinion on the stratigraphic ufulness of stromatolites in the Precambrian. Those who vstromatolites as sedimentary or biosedimentary structare today in the majority and stromatolites are preferaregarded as environmental rather than stratigraphic indtors. They do not represent fossils sensu strictu, but are rlithified associations of sediment and microbial mats. Nertheless, stromatolites bear witness to the early evolutiolife, as far back as 3.5 Ga, and may contain fossil microremains of that age. They occur in a vast range of shaand sizes, as microstromatolites (Fig. 1), recognisablein microscopic thin section, in small, patchy lithoherms, awithin widespread stromatolitic lithostromes, up to tenshundreds of metres in thickness and hundreds of kilotres in lateral extent (Fig. 2). Shallow pools and peritirealms or evaporitic and hydrothermal basins are envisaas the main sites of stromatolite growth. However, frthe Precambrian rock record, microbial mats thrivingdeep, aphotic conditions were also reported. In Archeanmatolites microfossil preservation is extremely exceptioStromatolites bearing microfossils are termed “biophorwhereas microbially influenced fossilised biosedimentstructures are named “biogenic” stromatolites. Non-biogestromatolites, precipitated chemically, and biogenic strotolites can be biophoric if they contain chemical precipitwhich has trapped and fossilised organisms in the enviment (comp. Altermann [2] and references therein).

W. Altermann, J. Kazmierczak / Research in Microbiology 154 (2003) 611–617 613

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Fig. 2. Field occurrence of Archean stromatolites: (A) Small domical to columnar stromatolite in partly silicified carbonate rocks of the 3.45 Ga WaawoonaGroup, Western Australia (scale in cm). (B) 2.7 Ga pseudocolumnar, laterally linked, silicified stromatolites in volcanic, tuffaceous rocks of the VentersdorpSupergroup, South Africa (40 cm long hammer handle for scale). (C) Giant stromatolitic domes of the 2.5 Ga Campbellrand Subgroup. These subscan attain over 50 m length and 20 m height and 2 m of synoptic relief and are parallel to palaeocurrents. The stromatolitic beds (reefs) are tracer tensof kilometers laterally.

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3. Criteria and methods for microfossil identification

Several workers attempted to set up criteria for recoging genuine Archean microfossils and distinguishing sfindings from younger fossilised bacterial contaminapseudofossils and artefacts [8,30]. To ensure the autheity of Archaean microfossils the samples must be of firmestablished Archean provenance and age, the fossilsbe indigenous to the rock and syngenetic with its desition (i.e., not introduced by later colonisation of cracand pores in the rock [42]), and allowing for morpholoical recognition of assured biological origin. Several linof positive evidence like fossil morphology, the presenof carbonaceous matter, isotopic signatures, biomarkersmineralogy need to be combined in such a testimony.rographic thin sections that can provide clear evidencthe relationship between fossil-like objects and theircompassing rock matrix, are best suited study objectsmust always be combined with at least the first three abmentioned positive pieces of evidence (morphology, carbisotopes). They may be supported by electron microsc(SEM), laser Raman spectroscopy, atomic force microsc(AFM) and isotopic investigations, performed preferablyindividual fossils.

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Techniques like SEM or AFM expose only the surfaof the rock and do not reveal the relationship of the sposedly biogenic structure to the rock itself, as petrograthin sections do. Petrographic studies and understandinthe diagenetic and metamorphic history of the samplehowever, crucial evidence and must be presented in oto demonstrate that the sample is potentially suitableauthentic microfossil preservation and is indeed microsiliferous. Laser Raman spectroscopy can demonstratethe microfossils in question are made of carbonaceouster. The crystallinity of carbon, if detectable, should actuacorrespond to the diagenetic and metamorphic historthe rock itself—a criterion that has rarely been fully dcussed yet, because of insufficient laser Raman analytechniques [23,31]. AFM usage on Precambrian microsils is still an experimental technique currently applied oto previously assured microfossil occurrences. Coccoidcrofossils investigated with the AFM, combined with lasRaman spectroscopy, were found to consist of kerogewalls composed of stacked, platy, angular polyaromaticdrocarbon subunits∼200 nm in size, oriented perpendicuto the cell walls [16]. It has yet to be demonstrated to wextent this feature is typical and characteristic of microfopreservation.

614 W. Altermann, J. Kazmierczak / Research in Microbiology 154 (2003) 611–617

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Although the identification of isotopic and organic bimarkers provides indispensable information on the earlytraces preserved in rocks, such studies are to be treatedcaution. Rocks can be colonised by microbial communilong after their formation, when exposed to subsurfacesurface environments, and such colonies can becomesilized by migrating fluids and their precipitates. Orgacompounds can be introduced into the rock by percolaground water. Younger bituminous matter and fluids canbe trapped in microscopic fluid inclusions, in minerals filliopen spaces, e.g., pores and cracks, when the rocks aposed to low hydrothermal fluid migration. Therefore, in sstudies on particular microfossils are better evidencebulk rock analyses, but are extremely difficult to performstructures of only a few µm across, and are thereforevery rare [13].

Taxonomic classification of Precambrian microfossilsbased on morphometrics of often badly preserved spmens, and on their morphological comparisons to represtatives of modern taxa. The main characteristics used in csification include shape and size of cells, form of filamand thallus, patterns of cell growth and division, presencabsence of extracellular sheaths or envelopes, form of ecellular structures and of wall ornamentation, and preseor absence of colonial organisation. Schopf [27] suggethat fossil septate filaments<1.5 µm wide can be regardeas probable bacteria and those>3.5 µm wide as probablcyanobacteria. The range between these two classesreferred to as “undifferentiated prokaryotes”. Coccoid mcrofossils larger than 60 µm in diameter were assigne“assured eukaryotes”. However, because the size rangextant and fossil bacteria, cyanobacteria and alga ovethis subdivision is not inevitably correct, nor do morpholoical similarities necessarily imply similar metabolism. Hoever, no better, unequivocal criteria have been found thus

Morphologically representative measurements andtistical comparison to extant species are thus fundameSimple coccoid forms, single or arranged in clusters,corresponding in size to extant species, must be treatedscepticism. This is especially valid if such structures arefound in the samples by means other than SEM or AFi.e., the relationship to embedding rock matrix is uncleand if no easily discernible cell walls are recognisable.ica often crystallises to spheroidal aggregates of a fewto sub-µm in diameter. Such spheroids may contain cafrom migrating bituminous fluids or simply from their CO2content. True coccoid microfossils may exhibit shapesflecting cell division and traces of the EPS surrounding sbenthic colonies. The morphology of filamentous fossilsfers more definite characteristics, including distinct termicells, cylindrical shapes with robust cell walls, septation,a typical range of widths (<0.5 to∼100 µm) and of lengthsof a few tens to a few hundred µm, to some degree compble to the sinuosity of the filaments [30].

Generally the microfossils found in Precambrian rotend to increase in size with time. Those found in ro

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of 3.5 to 3.0 Ga are often smaller than 10 µm in diamethose at around 2.5 Ga can be larger than 10 µm, andsured eukaryotes”>60 µm appear only in the ProterozoHowever, considering the scarcity of reports of autheearly Archean microbes, this observation might be facious. Schopf [29] has noticed that the early evolution ofis characterised by morphological conservatism, evidenin the extremely slow evolutionary progress of the prokaotes. This “hypobradytelic evolution” and the deficient fosrecord consequently imply that prokaryotes are of no stgraphic significance for the Archean.

4. The Archean fossil record

Extensive morphometric studies of∼2000 cells in∼180specimens have demonstrated a systematic correlatiotween cell shape, filament diameter, and taxon-speterminal cell morphology for each of the 11 filamentospecies described from the 3.46 Ga Apex Chert [2Suggestions that the Apex fossils might be thermallygraded remnants of ensheathed benthic colonies of coccyanobacteria [15] need further investigations on the oinal material. Interpretation of these fossils as remnantinorganic Fischer–Tropsch-type synthesis of carbon wihydrothermal systems [6] can only be considered wdemonstrated that such inorganic carbon synthesis canduce microfossil-like structures of similar isotopy and kegen crystallinity in chert.

From the early Archean fossil record, Schopf [30] hidentified only a few reports that fulfill the criteria listeabove. These microfossiliferous occurrences from eightto 3.5 Ga Archaean formations of Western Australia aSouth Africa can be accepted as authentic ancient fossilsprovide firm evidence that 3500 Myr ago microbial life wflourishing and presumably widespread. These oldestings contain spheroidal or filamentous microfossils [5,2428,32,35,38,39].One sampling location [5] from 3.45 Garocks of Western Australia could not be found again [30] aremains to be verified. Carbon isotopic analyses and laRaman spectroscopy, however, support the interpretatiothe structures found in this sample as authentic microsils. Negative carbon isotopic values, typical of Precambbiogenic kerogens, (up to−36❤) have been measured othe carbonaceous components and individual fossils ooldest of these findings. Few reports [18,22,37,38,41] wclassified [30] as being of possibly uncertain fossil ctent. Some of these findings, however, are now suppoby additional carbon isotopic and laser Raman spectrosanalyses and thus can, at least in part, be accepted as pble microfossils [1,18,30,38,41].

To the above listed early Archean findings, reports ofcertained younger Archean fossils can be added [4,14,17Colonial coccoid cyanobacteria have not yet been discovin rocks older than about 2.6 Ga, although their very eorigin is suggested by molecular phylogenetic analyses [

W. Altermann, J. Kazmierczak / Research in Microbiology 154 (2003) 611–617 615

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Fig. 3. Microfossils from stromatolitic, early diagenetically silicified limstones of the 2.55–2.52 Ga Campbellrand Subgroup, South Africa, in pgraphic thin section. (A) Faint fossil ghosts interpreted as remnants ofof entophysalidacean benthic coccoids assigned toEoentophysalissp. [4].(B) and (C) filamentous, cyanobacterial nonseptate sheaths assignEomycetopsiscf. filiformis [4].

Recognition of Neoarchean and Proterozoic fossils racomparably minor problems because fossils are more adant and often much better preserved. They can be so siin morphology to modern microbial taxa that both their bgenicity and biological affinities can be readily establishThe better preservation of Neoarchean to Proterozoic rplays an important role therein. The environmental setfor all Archean fossiliferous units ranges from shallow mrine intertidal to subtidal, to hydrothermal.

Most reports of Archean microfossils are from diagnetically silicified carbonates or primary cherts (Fig.Carbonate rocks are conventionally excluded as a potesource of microfossils because of the crystallization foof carbonate minerals, which is believed to be responsfor destruction of prokaryotic cell-sized structures. In oreported exception, the filaments described asSiphonophy-cus transvaalensiswere partly preserved in late diageneteuhedral dolomite crystals, in parallel with their presertion in chert [17]. These cyanobacteria-like filaments dispminute needles (originally aragonite?) within sheaths,were interpreted as possible remains of cyanobacterial cfication.

Non-silicified occurrences of carbonate rocks are rin early Archean successions, including the 3.5 Ga Wawoona Group. Thick and extensive stromatolitic carbonplatforms appear in the geologic record only at about 2.2.6 Ga and the mechanism of biocalcification and carboprecipitation is highly debated for the entire PrecambrWright and Altermann [43] reported on possible microbmediation in calcification and dolomitisation processesmicrobial laminites and oolites. Rates of sediment acmulation and organic production on Neoarchean carbo

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platforms were comparable to those on modern carboplatforms and in recent microbial mats [3,19]. The fidirect morphological evidence for biomineralisation by bthic coccoid Archean cyanobacteria was presented fromCampbellrand Subgroup of South Africa [14]. The biostrtures obtainable in the SEM images are essentially similacapsules and common mucilage sheaths of modern becyanobacteria classified within the orders Chroococc(particularly the family Entophysalidaceae) and Pleurocsales (comp. Fig. 4). The characteristic feature of all thcyanobacteria is the capsular organisation of their mucilnous sheaths surrounding individual cells and cell clusforming colonies. The process of early postmortem meralization in the ca. 2.6 Ga Neoarchean cyanobacprobably reflects the action of heterotrophic bacteria uthe dead cyanobacterial biomass. The lytic action of theerotrophic bacteria might have led to liberation of Ca aMg cations stored (complexed) in the cyanobacterial Eand glycocalyx during their lifetime. This, in turn, mighave enhanced precipitation of carbonate minerals withe extracellular polymers and in spaces occupied eaby the cytoplasm, by increasing calcium carbonate osaturation. It has been proposed [14] that taphonomicfossilisation processes similar, if not identical, to thoseing today were in operation in the early history of lifThe abundant cyanobacterial mats in the peritidal depoof Neoarchean formations suggest mass production ofgrained calcium carbonate by benthic coccoid cyanobteria. This process explains the finely laminated naturmost Archean (particularly stromatolitic) calcareous sements.

5. Conclusions

Microfossils from the Archean are extremely difficultidentify and are subject to continuous controversy. Archstromatolites, although evidencing early life on Earth, cnot be viewed as fossils sensu strictu. The earliest miscopically recognisable microfossils were reported from3.49 Ga Dresser Formation and from the 3.46 Ga Apex Cof the Pilbara craton, Australia. Although their biogenechas recently been questioned, whole rock carbon isotcompositions with RuBisCO-signatures and morphologaffinity of microfossils to recent cyanobacteria and bacria, together with laser Raman identification of carbon witthe fossil bodies, testify to their authenticity. Certainly, lin a more primitive form must have existed on Earthfore 3.5 Ga, but the key to proving it lies in finding oldrocks or in utilising new methods allowing identificationcryptic organic remnants. When extrapolating to extrarestrial conditions the difficulties in finding and recognisiArchean microfossils, the prospect of finding and identifymicrofossils in Martian samples seem extremely faint,undisputed results can only be obtained on samples broback to Earth’s laboratories.

616 W. Altermann, J. Kazmierczak / Research in Microbiology 154 (2003) 611–617

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Fig. 4. (A) SEM image of mucilage capsules from the∼2.6 Ga old Nauga Fm. (South Africa) cyanobacterial mat mineralized by calcium carbonateAl–Fe silicates. (B) Similarly mineralized modern capsules from Lake Vai Si’i, Tonga. (C) SEM image of etched section of the Archean mat, showinernsresembling capsular mucilage sheaths of modern coccoid pleurocapsalean cyanobacteria, like those shown in (D) from the rocky shore of Sulejow DentralPoland. (The Archean sample was taken north of the Orange River at Prieska, approximately at 29◦32′S/22◦40′E.)

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Acknowledgements

The Centre National de la Recherche Scientifique,Foundation for Polish Science, and Le Studium, Orléansacknowledged for financial support of this study.

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