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LETTERS

Large colonial organisms with coordinated growth in

oxygenated environments 2.1 Gyr agoAbderrazak El Albani1, Stefan Bengtson2, Donald E. Canfield3, Andrey Bekker4, Roberto Macchiarelli5,6,

Arnaud Mazurier7, Emma U. Hammarlund2,3,8, Philippe Boulvais9, Jean-Jacques Dupuy10, Claude Fontaine1,

Franz T. Fursich11, Francois Gauthier-Lafaye12, Philippe Janvier13, Emmanuelle Javaux14, Frantz Ossa Ossa1,

Anne-Catherine Pierson-Wickmann9, Armelle Riboulleau15, Paul Sardini1, Daniel Vachard15, Martin Whitehouse16

& Alain Meunier1

The evidence for macroscopic life during the Palaeoproterozoicera (2.51.6 Gyr ago) is controversial15. Except for the nearly

2-Gyrold coil-shaped fossil Grypania spiralis6,7

, which may havebeen eukaryotic, evidence for morphological and taxonomic bio-diversification of macroorganisms only occurs towards the begin-ning of the Mesoproterozoic era (1.61.0 Gyr)8. Here we report thediscovery of centimetre-sized structures from the 2.1-Gyr-oldblack shales of the Palaeoproterozoic Francevillian B Formationin Gabon, which we interpret as highly organized and spatiallydiscrete populations of colonial organisms. The structures areup to 12 cm in size and have characteristic shapes, with a simplebut distinct ground pattern of flexible sheets and, usually, a per-meating radial fabric. Geochemical analyses suggest that the sedi-ments were deposited under an oxygenated water column. Carbonand sulphur isotopic data indicate that the structures were distinctbiogenic objects, fossilized by pyritization early in the formation

of the rock. The growth patterns deduced from the fossil morpho-logies suggest that the organisms showed cell-to-cell signallingand coordinated responses, as is commonly associated with multi-cellular organization9. The Gabon fossils, occurring after the2.452.32-Gyr increase in atmospheric oxygen concentration10,may be seen as ancient representatives of multicellular life, whichexpanded so rapidly 1.5 Gyr later, in the Cambrian explosion.

Our samples come from the Francevillian Group,which belongs toa well-recognized lithostratigraphic succession, outcropping across35,000 km2 in southeastern Gabon11,12. This group is exposed in theintracratonic basins of Plateau des Abeilles, Lastoursville andFranceville (Fig. 1), and reaches a maximum thickness of about2,000 m.

The group consists of five unmetamorphosed and undeformed

sedimentary formations, FA to FE, bounded by conformable sur-faces11,12. The lower part of the sequence (FA Formation) comprisesfluvial deposits of a low-standsystem tract dominated by onshore-to-coastal sandstones. In the FB Formation, marine deltaic deposition isindicated by facies development and sedimentary structures such asload casts, water escape structures, cross-stratification and hum-mocky cross-stratification. Shallower water conditions are observedin the FC Formation, whereas subsequent deposits (FDand FE)show

intercalated volcanic and continental sediments accumulated duringthe ultimate filling phase of the basin (Supplementary Fig. 1).

1Laboratoire HYDRASA, UMR 6269 CNRS-INSU,Universite de Poitiers, 86022 Poitiers, France.2Department of Palaeozoology,Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden. 3Nordic Center for Earth Evolution, DK-5230 Odense M, Denmark. 4Department of Geological Sciences, University of Manitoba, Manitoba, R3T 2N2Canada. 5Departement Geosciences, Centre de Microtomographie, Universite de Poitiers, 86022 Poitiers, France. 6Departement de Prehistoire, UMR 7194 CNRS, Museum NationaldHistoireNaturelle, Paris,75005, France.7Societe Etudes RecherchesMateriaux, CRIBiopole,86000Poitiers,France.8Department of Geological Sciences,StockholmUniversity, SE-106 91 Stockholm, Sweden. 9Departement Geosciences, UMR 6118, Universite de Rennes, 35042 Rennes, France. 10Bureau de Recherches Geologiques et Minieres, 45060 Orleans,France. 11GeoZentrumNordbayern, Universitat Erlangen,Fachgruppe Palaoumwelt,D 91054 Erlangen,Germany. 12Laboratoire dHydrologieet de Geochimie de Strasbourg, UMR7517CNRS, 67084 Strasbourg, France. 13Departement Histoire de la Terre, UMR 7207 CNRS, Museum National dHistoire Naturelle, Paris, 75005, France. 14Departement de Geologie,Unite de Recherche Paleobotanique-Paleopalynologie-Micropaleontologie, Universite de Liege, Sart-Tilman Liege 4000, Belgium. 15Laboratoire Geosystemes, FRE 3298 CNRS,Universite Lille 1, 59655 Villeneuve dAscq, France. 16Laboratory for Isotope Geology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden.

Volcanic rocks of NGoutou

0 50 km

Gabon

Plateau des

Abeilles

Lastoursville

Basin

Ondili shoal

Okondja

Basin

Volcanic complex of NGoutou

Archean basement

Francevillian

Basin

Franceville

Phanaerozoic deposit

Francevillian group

Gneiss of Okanja

Gneiss of Ogoue

Gneiss and granite (Archaean)

Figure 1 | Simplified geological map of Gabon. Showing the Francevillianbasin (inset) and the location of the fossiliferous site (star) near the town ofFranceville.

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The lower part of the investigated FB2 section, where FB2 is theupper part of FB, outcropping near Franceville, consists of sandstonebeds deposited in channels near the fair-weather wave base in thelow-energy environment of a prograding delta. The topmost part ofthis section consists of an oxidized and stromatolitic hardgroundsurface. This is sharply overlain by a 5-m-thick deposit of finelylaminated horizontal black shales, interbedded with thin siltstonelayers, deposited by waning storm surge without any evidence forsubaerialexposure(SupplementaryFig. 1).The ageof theFB deposits

is well constrained to 2,1006 30 Myr (refs 1315), roughly con-temporaneous with the,2.222.10 Gyr Lomagundi marine positivecarbon-isotope excursion16 (see Supplementary Information andSupplementary Fig. 1) and about 200250 Myr after the first signifi-cant rise in atmospheric oxygen concentration10.

More than 250 pyritized specimens embedded within their sedi-mentary matrix were collected in situfrom at least 18 thin horizons,identified within the FB2 black shale lithofacies (SupplementaryFig. 2). In some cases, the layers containing the specimens werelocally coated with iron oxides, owing to oxidation of pyrite crystals.The specimens range in shape from elongated to nearly isodiametricforms, with occasional finger-like protrusions (Fig. 2, SupplementaryFig. 3). Their length and width range from 7 to 120 mm and from,5to 70 mm respectively, and their thickness varies from,1 to 10 mm.

We estimate a density of up to 40 specimens per m2, with forms ofdifferent sizes and shapes and disparate orientations occurringtogether (Supplementary Figs 3, 4).

We used micro-computed tomography (micro-CT)-based three-dimensional (3D) imaging to characterize the outer and innermorphologies of the structures (see Supplementary Information).Most specimens show a pattern of radial fabric at the outer edge oftheir undulate or lobate periphery (Figs 2, 3, 4ac, SupplementaryFigs 58); this is often curved, so as to meet the outer rim at a roughlyperpendicular angle. In some cases, the radial fabric does not reachthe outer rim (Fig. 4d), whereas in others it is simply lacking. Thecentral parts of the larger forms are commonly thrown into smooth,transverse folds, which do not reach the outer edge and which areexternally expressed as wrinkling of the structure (Figs 3, 4bc,

Supplementary Fig. 68, 11). Laminae of the host shale are drapedaround the folds (Supplementary Fig. 13), showing that the foldingoccurred before compaction. X-ray diffraction analyses show nomineralogical difference between the clay matrices in the specimensand the host shale (Supplementary Fig. 14, Supplementary Table 1).

Thelarger specimensoften alsocontaina central pyrite body (Figs 3,4c, d, Supplementary Figs 8, 11), which is developed differently.Sometimes it forms a median layer within the folded sheet (Sup-plementary Figs 68), but it is more often nodular (Figs 3b, 4cd,Supplementary Figs 8, 11), sometimes deflecting the transversefolds (Fig. 4c, Supplementary Fig. 11). We measured topographicthickness along geometrically homologous virtual sections, whichindicated progressive thinning towards the periphery (Supplemen-tary Figs 9, 10).

Differences in X-ray attenuation within the specimens are largelydue to the differential distribution of octahedral pyrite crystals. Theperipheral radialfabric is characterizedby pyrite-freeregionsexpressedin the microfabric as canals or slits (Supplementary Figs 12, 15).Secondary-ionizationmass-spectrometric analysis of the pyrite revealsverylightd34S values of about225% to230% in the fossilized sheets,with the central pyrite nodule tending towards heaviervalues of 5% to15%, particularly in theouter margins (Fig. 5, SupplementaryTable2).The sheet, which represents the main body of the fossilized structure,was therefore pyritizedduringearly diagenesis, when sulphate reducerswere in direct contact with the effectively unlimited sulphate pool ofthe overlying water column. The high fractionations suggest sulphateconcentrations in excess of 200 mM (ref. 17) (Supplementary Fig. 17).The pyritized nodules apparently formed later, from pore fluids more

depleted in sulphate, and the pattern of sulphur isotopes suggests that

b

a

Figure 2 | Examples of black shale bedding surfaces. a, b, Bearingmacrofossils in colony form from the FB2 level. Scale bars, 1.0 cm.

b

c

a

Figure 3 | In situ macrofossil specimen from the FB2 Formation. a, Lowerside of the fossil (top) with its impression left in the black shales (bottom),showing peripheral radial fabric and wrinkled appearance. b, Micro-CT-based virtual reconstruction (volume rendered in semi-transparency),showing radial fabric and two inner pyrite concretions. c, Longitudinal

virtual section running close to the estimated central part of the specimen,evidencing the fold pattern. Scale bars, 1.0 cm.

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pyritization began at the centre and continued towards the outer mar-gins, during which process the remaining sulphate became progres-sively more depleted in light isotopes. The sulphur isotope patternsthussupport the interpretation that the pyritized sheets represent earlydiagenesis of original biological fabric, whereas the occasional centrallump of pyrite is a later, post-burial, diageneticfeaturethatis notlikelyto reflect original morphology.

The differences in the organic carbon d13C content recordedbetween five specimens and their associated host shale sediment alsosupport the fossilized structures representing a distinct organic entity(Supplementary Table 3). Plants and biomineralized animal tissuesof the Phanaerozoic eon are commonly pyritized; pyritization of softtissues is rare but typically results in faithful replication. This preser-vation is thought to be favoured by a low content of organic mole-cules and high content of reactive iron in the pore-waters18.

We find no evidence to support an inorganic origin of the struc-tures from the FB2 black shale level, whether concretions resultingfrom epitaxic/crystal growth processes, or features of diagenetic,sedimentary, hydrothermal, or tectonic origin. There is a superficialresemblance between the Gabon structures and the Ediacaran dubio-fossil Mawsonites spriggi, which has been interpreted as a sand vol-cano interacting with biomats19; however, this interpretationaccounts for neither the fine internal radial fabric nor the inner fold

pattern of the Gabon fossils, and there is no structural evidence ofsediment injection in association with the fossils. The Gabon fossilsalso resemble radially growing pyrite or marcasite crystals, or pyritesuns, whichare occasionally foundin Phanaerozoic shales. However,a micro-CT-based comparison of the inner structures clearly showsthat the pyrite suns have a much more regular and linear radialfabric than the Gabon specimens, and that this fabric extends allthe wayto the centre of thestructure, without any evidence of flexiblefolding (Supplementary Fig. 16). Indeed, we are unaware of anyinorganic processes that can generate the style of flexible foldingandirregular radialfabric that we observe in theGabonfossils(Fig.4).

The accumulated evidence suggests thatthe structures are biogenic.The fold pattern seen in the centre of most of the specimens indicatesdeformation of a flexible sheet, implying an originally cohesive struc-ture of organic composition. The radial fabric is commonly deflectedto meet the rim of the specimen, suggesting that the original materialwas growing by peripheral accretion of flexible organic matter. Weconclude that the Gabon structures fulfil the general criteria of bio-genicity applied to fossil-like forms in the early rock record20

(Supplementary Table 4). The presence of abundant organic matterin the FB Formation21,22 (Supplementary Table 5), including steranesof eukaryotic origin23, is consistent with this interpretation.

We consider it most likely that these structures represent fossilizedcolonial organisms. Bacterial colonies growing on surfaces are knownto coordinate their behaviour, resulting in regular shapes anddistinctfabrics9; radial fabrics are common, and are thought to be due torepulsive chemotaxis24. Most studies of bacterial colony growth havebeen done on monocultures in Petri dishes, where colonies exceedcentimetre size9. In nature, fairy-ring colonies, formed by cyano-bacteria and diatoms and reaching a diameter of 15 cm, have been

a b c d

a b c d

a b c d

a b c d

Figure 4 | Micro-CT-based reconstructions and virtual sections of fourspecimens from the FB2 macrofossil record of Gabon. Samples show adisparity of forms based on: external size and shape characteristics;peripheral radial microfabric (missing in viewd); patterns of topographicthickness distribution; general inner structural organization, includingoccurrence of folds(seenin views b and c) andof a nodular pyriteconcretionin the central part of the fossil (absent in views a and b). a, Originalspecimen. b, Volume rendering in semi-transparency. c, Transverse (axial)two-dimensional section. d, Longitudinal section running close to theestimated central part of the specimen. Scale bars, 5 mm. Specimens fromtop to bottom: G-FB2-f-mst1.1, G-FB2-f-mst2.1, G-FB2-f-mst3.1, G-FB2-f-mst4.1.

1 mm30

15

34S

Figure 5 | Section through specimen G-FB2-f-mst4.3. d34S values(colouredspots, seescale) are measured in the central pyritenodule (centre)and surrounding sheet material (top and bottom) by secondary-ionizationmass spectrometry. See Supplementary Information.

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reported25. Nonetheless, structures similar to those from Gabon areunknown in the available fossil record and, because of their complexinner structural morphology and the sterane signature in the FBrocks, it is also possible that they represent colonial eukaryotes.

Microbial mat-forming communities, including organisms whosephototactic behaviour modifies the mat shape, are inferred to havebeen prevalent in marine and lacustrine environments from the earlyArchaean eon26. Because of their sediment-binding properties, suchmats often leave characteristic structures in carbonates and siliciclas-

tic rocks. Such structures, however, including those formed in shalesand mudstones, do not resemble the Gabon fossils27. Colonies withregular fabric resulting from coordinated-growth behaviour, as weinfer for the Gabon fossils, represent a degree of organization differ-ent to that of such mat-forming communities. They require cell-to-cell signalling and coordinated responses, akin to that required formulticellular organization9. The Gabon fossils represent the earliestevidence for such signalling and coordinated-growth behaviour onthe scale of macroorganisms.

One fundamental selective advantage of multicellularity is largesize28, butambient oxygen levelsmust be high enoughto allow aerobicorganisms to grow large. Our iron-speciation analyses reveal lowratiosof highly reactive iron to total iron (FeHR/FeT)

29, consistent withsediment deposition under an oxygenated water column (Sup-

plementary Fig. 18). This implies that these fossil organisms, livingon the sediment surface, were likely to engage in aerobic respiration.This is consistent with the timing of deposition, some 200 to 250 Myrafter the first accumulation of oxygen into the atmosphere10,30.

Although we cannot determine the precise nature and affinities ofthe 2.1-Gyr macroorganisms from the Francevillian B Formation ofGabon, we interpret these fossils as ancient representatives of multi-cellular life, which expanded so rapidly 1.5 Gyr later.

METHODS SUMMARY

We assessed textural relations between the pyritized sheet and the shale matrixembedding the macrofossils on sections, using a Nikon Eclipse E600. We carried

out scanning electron microscopy on a JEOL 5600 LV, equipped with an Oxford

EDX for mineralogical analyses. We obtained X-ray diffraction patterns fromrandomly-oriented powders and oriented preparations using a PANalyticalXPert diffractometer(Ni-filtered Cu-Ka radiation),equipped withan accelerator

detector (2u 2h analysis angle).

We ran high-resolution micro-CT on X8050-16 Viscom AG equipment. Wemade reconstructions using DigiCT v.2.3 (Digisens), 64-bit version, running ona 2.5GHzDell T7400 PrecisionWindowsXP 64workstationwith 32GB ofDDR

RAM and two NVIDIA graphic cards (Quadro FX 5600 and Telsa C870). Wecarriedout virtual sections and3D renderingon AVIZO v.5(MercuryComputer

Systems). We carried out SRXTM tomographic microscopy at the X02DATOMCAT beamline of the Swiss Light Source at the Paul Scherrer Institute(http://www.psi.ch/).

We studied organic matter using Rock-Eval III pyrolysis (Oil Show

Analyzer). We took isotopic measurements (d13Ccarb) on a VG Sira 10 triplecollector mass spectrometer. We investigated iron speciation using the sequen-

tial extraction protocol, and determined sulphide concentrations by the chro-mium reduction method (CRM). We measured the concentration of iron in all

iron fractions, except for pyrite, by atomic absorption spectrometry. We mea-suredthe d34S compositionof bulk rock on Ag2S precipitates from samplesof thesulphide that was liberated by CRM. We added about 200mg to a tin cup with

V2O5 and combusted it using a Thermo elemental analyser coupled via aConflow III interface to a Thermo Delta V Plus mass spectrometer. We analysedS isotopes (32S, 33S and 34S) by secondary-ionization mass spectrometry using a

Cameca IMS1270e7.

For further details of sample treatment and analytical procedures, seeSupplementary Information.

Received 29 March; accepted 4 May 2010.

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Supplementary Information is linked to the online version of the paper atwww.nature.com/nature.

Acknowledgements We thank the Ministry of Mines, Oil, Energy and HydraulicResources and the General Direction of Mines and Geology of Gabon forcollaboration and assistance, and the French Embassy at Libreville and the FrenchMinistry for Foreign Affairs for support. We thank F. Mayaga-Mikolo, D. Beaufort,

B. Cost,D. Thieblemont,F. Pamboand H. Sigmund fordiscussions.For assistance inGabon and France, we acknowledge S. Accolas, T. Bonifait, B. Braconnier,N. Dauger, F. Duru, D. Fabry, F. Haessler, M. Jouve, G. Letort, D. Paquet, J.-C.Parneix, D. Proust, M. Stampanoni and X. Valentin. We also acknowledge the

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Institut Francais du Petrole, the Swiss Light Source (TOMCAT beamline) at thePaul Scherrer Institute, and the Centre de Microtomographie at the University ofPoitiers (CdMT).Nordsim is operated under an agreementof theJointCommitteeof the Nordic Research Councils for Natural Sciences (NOS-N), with further

funding from the Knut and Alice Wallenberg Foundation; this is Nordsimcontribution 256. Research was supported by the French CNRS-INSU, the Bureaude Recherches Geologiques et Minieres (BRGM), the Danish National ResearchFoundation and the Swedish Research Council.

Author Contributions A.E.A. conceived andheaded theproject. A.E.A., S.B., D.E.C.,E.H., A.B., R.M., J.-J.D., P.J. and A.Meunier designed research. A.E.A., A.Mazurier,E.H., F.O.O. and P.S. did field research. A.E.A. and F.O.O. analysed sedimentology.

A.E.A., S.B., F.T.F., P.S. and D.V. analysed morphology. A.E.A., S.B., R.M. andA.Mazurier carried out microtomographic analyses. E.J. analysed palynology.

A.E.A., C.F., F.O.O.and A.Meunier analysed mineralogy. S.B., D.E.C., A.B., E.H., P.B.,A.-C.P.-W., A.R. and M.W. carried out isotope and geochemical analyses. F.G.-L.

provided geological samples. A.E.A., S.B., D.E.C., A.B., R.M., A.Mazurier, E.H., P.B.,C.F., F.T.F., F.G.-L., P.J., E.J., F.O.O., A.-C.P.-W., A.R., D.V., M.W. and A.Meunieranalysed data. A.E.A., S.B., D.E.C., R.M. and E.H. wrote the main part of themanuscript. A.B., A.Mazurier, P.B., J.-J.D., C.F., F.T.F., F.G.-L., P.J., E.J., A.-C.P.-W.,A.R., D.V., M.W. and A.Meunier provided critical input to the manuscript.

Author Information The repository of the fossils is the Department ofGeosciences, University of Poitiers, France. Reprints and permissions informationis available at www.nature.com/reprints. The authors declare no competingfinancial interests. Readers are welcome to comment on the online version of this

article at www.nature.com/nature. Correspondence and requests for materialsshould be addressed to A.E.A. ([email protected]).

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1 - The Francevillian Group and the FB2 section

Figure S1 | a, Lithostratigraphy of the Palaeoproterozoic Francevillian group with the fiveFormations (FA to FE) and age constraints shown. b, Detailed stratigraphy of the FB2 section

outcropping near the town of Franceville, showing the macrofossil-bearing levels (black

shales). c, Stratigraphic evolution of

13

Ccarb values and of total organic carbon (TOC, wt. %)contents (see Tab. S5).

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Two Sm-Nd isochrons on clay minerals formed during the very early diagenesis give the

FB Formation an age of 2099 115 million years (Ma) (Bros et al., 1992). Zircons from the

tuff in the overlying FD Formation provided a 2083 5 Ma SHRIMP U-Pb syndepositional

age (Hoori et al., 2005). The Oklo diagenetic uranium deposit at the FA-FB boundary has

been dated at 2050 30 Ma by using U-Pb method (Gancarz, 1978). Taken together, these

data indicate the depositional age for the Francevillian B Formation near 2100 30 Ma. This

is supported by the highly positive 13C values of the carbonate fraction of the FB2 black

shales (Fig. S1), the range of which (+5.5 to +9.6) is consistent with deposition during

the ~2.22-2.10 Ga Lomagundi seawater positive carbon isotope excursion (Bekker et al.,

2008).



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2 - The site and the macrofossils

Figure S2 | a, The Francevillian B2 site outcropping near the town of Franceville, Gabon. b,The transition between the cemented sandstone beds and the black shales. c, The 5 m-thick

finely-laminated fossiliferous black shales. Scale bar, 50 cm.



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Figure S3 | Black shale bedding surface bearing macrofossils from the FB2 levelphotographed in situ. The disparity of spatially close and serially repeated forms is evident.

Scale bar, 10 cm.



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Figure S4 | a, Black shale surface from the FB2 level bearing macrofossils. In this case,density approximates 40 specimens/m2. b, c, d, Details showing the disparate orientation of

differently sized and shaped structures (as indicated by arrows). The surface is locally coated

with iron oxides. Contact deformation of the surrounding black shale sediment with the

structures is occasionally seen. Scale bar, 10 cm.



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Figure S5 |Macrofossil specimen (G-FB2-f-mst1.3) from the FB2 Formation. a, Lower sideof the specimen (top) with its counterpart (impression) left in the black shales (bottom). b,

Micro-CT-based 2D reconstruction (volume virtually rendered in coloured semi-transparency;

for technical informations, see section 3 below) showing peripheral radial fabric. Scale bars, 1

cm.



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Figure S6 | Macrofossil specimen (G-FB2-f-mst2.4) from the FB2 Formation. a, Lower sideof the specimen (right) with its counterpart (left) showing peripheral radial fabric and folded

appearance. b, Micro-CT-based 2D (left) and 3D (right) virtual reconstructions showing radial

fabric and the inner fold pattern. c, Longitudinal section running close to the estimated central

part of the specimen evidencing the extent of the central fold. Scale bars, 1 cm.



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Figure S7 | Macrofossil specimen (G-FB2-f-mst2.2) from the FB2 Formation. a, Lower (right)and upper (centre) sides of the specimen with its counterpart (left) showing wrinkled

appearance and, to a minor extent, peripheral radial fabric (notable on the lower side). b,

Micro-CT-based 2D (left) and 3D (right) virtual reconstructions showing radial fabric and a

particularly complex inner fold pattern. c, Longitudinal section evidencing the multiple,heterogeneous folds. Scale bars, 1 cm.



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Figure S8 | Macrofossil specimen (G-FB2-f-mst3.10) from the FB2 Formation. a, Upper sideof the specimen showing peripheral radial fabric and folded appearance. b, Micro-CT-based

2D (left) and 3D (right) virtual reconstructions showing radial fabric, folds, and the pyrite

concretion filling the central part. c, Longitudinal section evidencing the fold pattern and the

position of the pyritic body. Scale bars, 1 cm.



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3 - Microtomography (micro-CT and SR-micro-CT)

The macrofossils have been studied by means of high-resolution microtomography (micro-

CT) at the Centre de Microtomographie of the University of Poitiers, France. The equipment

used, a X8050-16 Viscom AG (1004x1004 camera), is a multi-scale X-ray inspection

system which allows the analysis of variable sized objects up to a diameter of 300 mm.

Depending on the specimens, scan parameters were 100 to 120 kV, 0.5 to 0.8 mA current,

1500 to 1800 views, 32 integrations by view, 16-bit tif images. Reconstructions have been

done at theEtudes Recherches Matriaux company (www.erm-poitiers.fr) using the software

DigiCT v.2.3 (Digisens) 64-bit version running on a 2.5 GHz Dell T7400 Precision Windows

XP 64 workstation with 32 GB of DDR RAM and two NVIDIA graphic cards (Quadro FX

5600 and Telsa C870). This workstation allows using of the Digisens acceleration plug-ins for

tomographic reconstruction, SnapCT, which takes advantage of the GPU processing

capabilities. The final volumes were reconstructed in 992x992 formats with isotropic voxels.

The spatial resolution varied from 17 to 83 m3. Virtual sections, 3D rendering and

animations (see the attached four movies produced by A.Ma.) were performed by means of

AVIZO v.5 (Mercury Computer Systems Inc.) 64-bit version.

Two specimens (G-FB2-f-mst1.1 and mst3.8) have been also studied by means of

synchrotron radiation X-ray microtomography (SR-micro-CT) at the tomography station of

the Materials Science beamline (TOMCAT;

http://sls.web.psi.ch/view.php/beamlines/tomcat/index.html) of the Swiss Light Source set at

the Paul Scherrer Institute (http://www.psi.ch/), Villigen, Switzerland. In order to optimize the

signal-to-contrast ratio, the X-ray energy was set at 40 keV, because of the mineral

composition (e.g., mostly pyrite; Fig. S15). The magnification of the X-ray microscope was

10x or 20x. On-chip binning (2x) was selected to improve the signal-to-noise ratio for the 20x

scans. The projections (1001 or 1501, depending on magnification; 550 to 700ms exposure

time) were made over 180, and thus online post-processed and rearranged into flat- and

darkfield-corrected sinograms. Reconstructions were performed on a 16-nodes Linux PC farm

using highly optimized filtered back-projection routines. The reconstructed voxels are

isotropic and have a size of 0.74 m.

Topographic thickness variation has been assessed on the most suitable specimens along

geometrically homologous (usually "parasagittal") virtual sections. The results provide a

coherent pattern of symmetrical structural heterogeneity. Two examples are shown in Figs. S9

and S10.



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Figure S9 | Micro-CT-based topographic thickness variation (in m) and cross-sectionaloutline assessed along three virtual sections (different colours) parallel to the main axis in the

specimen G-FB2-f-mst1.1. Note the close pattern shown by the two lateral sections (blue and

red) and the distinct outline of the thicker intermediate section (green) running closer to the

central part of the fossil. Scale bars 5 mm.



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Figure S10 | Micro-CT-based topographic thickness variation (in m) and cross-sectionaloutline assessed along two virtual sections running through the central part of specimen G-

FB2-f-mst2.4. The external profile of the specimen suggests an inwards compaction of the

original structure involving one of its two long margins. Note the resemblance between the

two profiles and the relative position, shape and extent of the two folds. Scale bars, 5 mm.



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Figure S11 | Micro-CT-based imaging of the structural fold patterns shown by seven selectedspecimens from the FB2 Formation (axial virtual sections). a, G-FB2-f-mst2.1. b, G-FB2-f-

mst2.2. c, G-FB2-f-mst2.4. d, G-FB2-f-mst3.1. e, G-FB2-f-mst3.2. f, G-FB2-f-mst3.4. g, G-

FB2-f-mst3.10. Scale bars, 5 mm.



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Figure S12 | SR-micro-CT-based 3D reconstruction of a lateral portion of a specimen fromthe FB2 Formation (G-FB2-f-mst.3.8) showing radial microfabric. The long axis of the

investigated sample (from upper left to lower right) is approximately parallel to the long axis

of the specimen. The upper and lower surfaces of the sample correspond to the two opposite

surfaces of the specimen; the other surfaces (two cylindrical and two flat) are artificial,

formed by the boundaries of the SR-micro-CT scan. Note the distribution of the octahedral

pyrite crystals and their absence in a sediment-filled area forming narrow slits through the

structure. Crystal size decreases towards periphery. Scale bar, 100 m.



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4 - Composition of macrofossils

Textural relations between a pyritized sheet and the sediment

A section normal to bedding (Fig. S13) capturing the microstructure of the shale matrix

shows that the shale laminae are draped around the folds of the pyritized sheet. This confirms

that the structures are pre-compactional folds rather than features formed during late

diagenesis.

Figure S13 |Section of a specimen from the FB2 Formation (G-FB2-f-mst2.6) normal tobedding, photographed in reflected, plane-polarized light. a, Complete section of the pyritized

sheet showing general relationships between folded sheet and shale lamination. b, Detail of

fold concavity showing that shale laminae do not transverse into sheet structure. Scale bars,

2.5 mm.



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X Ray Diffraction

As shown in Figure S14a, three samples were extracted from the host sediment (1) and

from the edge (2) and the centre (3) of a pyritic body of a specimen from the FB2 Formation

(G-FB2-f-mst2.1). The clay fraction was concentrated using centrifugation after gentle

grinding. XRD patterns were obtained from randomly-oriented powders (Fig. S14b) and

oriented preparations (Fig. S14c) using a PANalytical XPert diffractometer (Ni-filtered Cu-

K radiation) equipped with accelerator detector (2 2 analysis angle). Analytical conditions

were as follows: 40 kV, 40 mA; 0.020 2 scanning step 45 sec counting time per step; 2.5-

65.0 2 and 2.0-30.0 scanning angular ranges for randomly oriented powders and oriented

mounts, respectively. As seen in Table S1 (below), there is no significant difference in clay

mineralogy between the three sampled spots.



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a

0

400

8001200

1600

2000

2400

2800

3200

3600

4000

4400

4800

5200

5600

6000

6400

6800

7200

7600

8000

84008800

9200

9600

10000

5 10 15 20 25 30 35 40 45 50 55 60 65

Position (2*thta)

Intensit(cps)

-4,2

6

Qz

-14,2

0

Ch

-10,0

0

I

-7,0

8C

h

-3,5

5

Ch

-3,1

3

Py

-2,7

1

Py+G

-2,5

8

C+I

-2,2

5

C+I

-2,2

1

Py

-1,8

0

Py+Go

-1,5

6

Py+Go+C

-1,5

0

Py+Go+C

-4,1

8

Go

-2,4

2

Py

-1,9

1

Py+G

-1,8

2

Q+C

-1,6

3

Py

-10,6

0

ML

-5,0

1

I

-3,3

4

Qz

-1,6

9

Go

-1,4

5

Py+Go

-4,7

2

Ch-4,4

9

I

-3,7

2

Do

-2,5

8

Ch+I

-2,4

5Q

-1,7

2

Go

-2,4

5

Go

-3,2

0

I

-2,9

9

I

-2,8

9

Do

-2,2

8

Q

-2,1

9

Do

-1,5

4

Q+Do

-2,1

2

Q

-1,9

8

Q-1,8

2Q

+Ch

-1,67

Q

-1,4

5

Q-1,8

2Q

+

Ch

-2,0

2

Do

-1,7

8

Do

-1,6

6

Q+Ch

-1,4

9C

h+I+D

o

1

2

3

b

0

400

800

1200

1600

2000

2400

2800

3200

3600

4000

4400

4800

5200

5600

6000

6400

6800

7200

7600

8000

8400

8800

9200

9600

10000

2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

Position (2*thta)

Intensit(cps)

-

4,2

6

Qz

-

14,2

0

Ch

-

10,0

0

I

-

7,0

8C

h

-

3,5

5

Ch

-

3,1

3

Py

-

4,1

8

Go

-

10,6

0

ML

-

5,0

1

I-

3,3

4

Qz

-

4,7

2

Ch

1

2

3

-

3,3

34

I

c



23/37

Figure S14 | Mineralogical composition of the samples extracted from the pyritized body andits host sediment of specimen G-FB2-f-mst2.1 from the FB2 Formation. a, Sampled sites; 1:

host sediment (arrow indicates the counterprint of the specimen); 2, edge; 3, central part of the

specimen. Scale bars, 1 cm. b, XRD patterns of randomly oriented powders. c, XRD patterns

of oriented preparations in the air-dried state. Chlorite (Ch), Illite/Smectite mixed-layer (ML);

Illite (I); Quartz (Q), Goethite (Go), Pyrite (Py), Dolomite (Do).

sediment

(see Fig.

14a-1)

specimen

(see Fig. 14a-2-3)

edge centre

bulk mineral components (see Fig. 14b)

Quartz ++++ +++ ++Pyrite ++ ++

Goethite + ++

Dolomite +

Chlorite ++ ++ ++

mixed-layer (Illite/Smectite) + + +

Illite + + +

phyllosilicates of clay fraction (see Fig. 14c)

Chlorite +++ +++ +++

mixed-layer (Illite/Smectite) ++ ++ ++

Illite +++ +++ ++

Table S1 | Mineralogical composition of the G-FB2-f-mst2.1 specimen from the FB2Formation. Relative quantities are appreciated using the intensity of the representative XRD

peaks.

Scanning Electron Microscopy (SEM) and Energy Dispersive Analysis System (EDX)Beside the structural investigations performed at infra-micrometric level by means of SR-

micro-CT (Fig. S12), the mineral composition of the specimens, notably at the level of their

periphery, has been analysed at the Department of Geosciences at the University of Poitiers

by using a scanning electron microscope (SEM) JEOL 5600 LV equipped with an Oxford

energy dispersive analysis system (EDX). The content of major elements has been normalized

using silicate standards. Analytical conditions were 15 kV, probe current 6.10-10 A.

An example of SEM-EDX results (specimen G-FB2-f-mst2.1) is provided in Fig. S15.



24/37

Figure S15 | SEM-EDX analysis of the lobate outer edge of a specimen from the FB2Formation (G-FB2-f-mst2.1) showing radial microfabric. a, General view (left) and details of

the areas within (lobe) and between (sediment) two lobate peripheral structures. b, Elemental

composition of the lobe showing high content of sulphur (S) and iron (Fe). c, Elemental

composition of the intermediate zone filled by clayey sediments.



25/37

Secondary Ionization Mass Spectrometry (SIMS)

Specimen G-FB2-f-mst4.3 was mounted in a 25 mm epoxy disc, coated with 30 nm gold

and inserted into the ion microprobe sample holder together with pre-polished and coated

pieces of sulfide standards (Crowe & Vaughan, 1996): Ruttan pyrite (34SCDT = +1.2 ),

Balmat pyrite (34SCDT = +15.1 ), and an in house mass independently fractionated

standard, 248474, from the Isua greenstone belt (34SCDT = +2 ; 33S =+ 3.2 ). S isotopes

(32S, 33S and 34S) were analysed using a Cameca IMS1270e7 (SIMS) located at the Swedish

Museum of Natural History, Stockholm (NordSIMS facility). Analytical methods and

instrument parameters were similar to those used by Whitehouse et al. (2005) and Kamber

and Whitehouse (2007). Briefly at +10 kV, ca. 2 nA Cs+ primary beam was operated in

critical focussing (Gaussian) mode with a 5 m raster to generate a ca. 10 m diameter

analytical area. The primary beam was operated together with a normal incidence electron

flooding gun for charge compensation, -10kV secondary beam, software (Cameca CIPS

version 5) automated centering of field aperture and simultaneous detection in three Faraday

detectors at an effective mass resolution of ca. 4500 on the 33S channel, sufficient to resolve

33S from 32S1H. The NMR field controller was utilised to ensure reproducibility of the

secondary ion signal during the analytical session.

The pyrite isotope standards were analysed several times, bracketing analyses of sulfides

of unknown isotopic composition, with the Ruttan pyrite used as the primary standard and the

other two standards as monitors. External precision on the 34SCDT values is ca. +0.6 (2 std

deviations) based on the Ruttan standard analyses. The results are shown in Tab. S2.

Sample ID32

S cps34

S/32

S sig % 34

SCDT 1 s.d.

(x106)

surrounding sheet material_2-1 740 0.042879 0.029 -27.39 0.32


surrounding sheet material_2-3 730 0.042859 0.031 -27.85 0.34surrounding sheet material_2-4 739 0.042893 0.030 -27.07 0.33















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central pyrite nodule_1-1 736 0.044267 0.025 4.10 0.29

central pyrite nodule_1-2 738 0.043833 0.029 -5.76 0.32


central pyrite nodule_1-4 761 0.043452 0.027 -14.40 0.30central pyrite nodule_1-5 738 0.043386 0.028 -15.90 0.31




































27/37






















































28/37


























Table S2 |34S values (average 1 s.d.) obtained by means of Secondary Ionization MassSpectrometry (SIMS) on a longitudinal section running through the central part of a specimen

from the FB2 Formation (G-FB2-f-mst4.3) and sampling at 150 sites its central pyrite nodule

and the surrounding sheet material, till the marginal edge of the specimen (see also Fig. 5 in

the main text).

Mass Spectrometry

Five fossilized specimens from the FB2 Formation and their associated host shale sediment

were analysed for 13C content at the Institute for Geology and Geochemistry (IGG),

Stockholm University (courtesy of H. Sigmund). The average results are shown in Tab. S3.

Sample ID 13

C () 13

C () diff. ()

sediment specimen

s1 -27.83 -33.32 5.49

s2 -28.97 -34.65 5.68

s3 -32.72 -33.35 0.63

s4 -11.74 -27.16 15.42

s5 -22.44 -30.77 8.33



29/37

Table S3 |13C values ( V-PDB) measured on five specimens from the FB2 Formation andtheir associated host shale sediment.



30/37

5 - Criteria of biogenicity

Figure S16 | Micro-CT-based axial virtual sections showing the inner structural organizationof a specimen from the FB2 Formation compared with a non-biological object. a, A pyrite

sun formed by radially growing crystals similar to colloform pyrite texture (rev. in Barrie et

al., 2009). b, The peripheral radial fabric and the central folds characterizing the specimen G-

FB2-f-mst2.1. Scale bars, 1 cm.



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Criteria of antiquity

A Structures must occur in rocks of known provenance (in situ)

B Structures must occur in rocks of established age, ideally dated directly by radiometric techniques

C Structures must be indigenous and syngenetic with the primary fabric of the host rock, i.e., they m

physically embedded within the rock, not introduced by post-depositional fluids

D Structures should not occur in high-grade metamorphic rocks

E The geological context of the host rock must be well understood at regional scale

F Fossils should not be significantly different in colour from that of the rock matrix

G There should be evidence for organo-sedimentary interaction

Criteria of biogenicity

H Structures should exhibit biological morphology that can be related to extant cells, structures or activities

I More than a single step of biology-like processing should be evident. These steps may take the form of :

biominerals

geochemical fractionations of isotopes (sulphur and

specific organic comJ Structures should occur within a geological context that is plausible for life, i.e., at temperatures and pr

that extant organisms are known to survive

K - Structures should fit within a plausible evolutionary context

L - Structures should be abundant and ideally occur in a multi-component assemblage. Ideally they should sho

colonial/community behaviour

Table S4 | Condition shown by the 2.1 Ga FB2 black shales outcropping near Franceville, Gabon, and their fowith respect to some among the most common criteria considered to assess antiquity and biogenicity (adapted

criteria ranging from "fully met condition" (+++) to "condition not met" (), through "uncertain condition" (~condition mostly met; + = condition partly met.

www.nat ure.com/ nat ure


32/37

6 - Geochemical and isotopic data (bulk sediment)

Total organic carbon content and carbon isotopes

The origin of the organic matter (OM) cannot be identified from the bulk data obtained

from Rock-Eval pyrolysis because of the high maturity of the samples. Several authors have

inferred algal and cyanobacterial origins for organic matter in the black shales of the FB

Formation (Cortial et al., 1990; Mossman et al., 2001). A contribution from cyanobacteria

and marine algae to the OM of the FB Formation is also supported by biomarkers (Dutkiewicz

et al., 2007). Notably, a eukaryote signature indicated by steranes has been proposed to be

responsible for very high OM content in the FB Formation (Dutkiewicz et al., 2007).

The total organic carbon (TOC) content (wt. %) of three samples from the lower sandstone

beds of the FB2 unit and 10 samples from the laminated black shales of the FB2 fossiliferous

horizon are shown in Tab. S5.

Carbon isotopic values for 10 black shale samples are shown using standard notation in

units of relative to V-PDB standard in Tab. S5. The 13C values of the carbonate fraction

(13Ccarb) were measured on CO2 released by reaction of 50 to 300 mg of fine-grained powder

with 100% H3PO4 at 50C (Stable Isotopes Laboratory, Department of Geosciences at the

University of Rennes 1). H2S released during reaction between sulphide grains and H3PO4

was eliminated by reaction with Ag3PO4 at ca. 60C for 5 minutes. Isotopic measurements

were done on a VG Sira 10 triple collector mass spectrometer. Repeated analyses of internal

lab standard Prolabo Rennes gave a mean 13C value of -9.720.03 (1s, n=14), close to the

accepted value of -9.692. No correction was added to the measured values, and the

analytical uncertainty is estimated lower than 0.1. The studied carbonate-containing rocks

are characterized by carbonate content between 2.9 and 11.4 wt. % and 13Ccarb values

between +5.5 and +9.6 V-PDB (Fig. S1c), which are typical for marine carbonates

deposited during the 2.22-2.10 Ga Lomagundi seawater positive carbon isotope excursion

(Schidlowski et al., 1975; Bekkeret al., 2008).



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Sample

13

Ccarb

( V-PDB)

TOC (wt. %)

(rock-eval)

carbonate

(wt. % carb)

(calcimetry)

FB9-02 0.12 0

(sandstone)

FB9-04 0.39 0

(sandstone)

FB9-06 0.39 0

(sandstone)

FB9-08 7.3 2.30 2.9

FB9-09 6.8 1.79 6.4

FB9-10 5.6 3.41 8.2

FB9-11 5.6 1.98 10.0

FB9-12 5.9 2.00 11.4

FB9-13 7.0 3.41 5.2

FB9-14 5.5 2.20 7.1

FB9-15 6.5 2.12 7.4

FB9-16 9.6 2.47 3.3

FB9-17 6.1 1.72 8.4

Table S5 |13Ccarb values ( V-PDB), total organic carbon (TOC, wt. %), and carbonatecontent of samples from the FB2 section (cf. Fig. S1c).

Isotopes of sulphurThe

34S composition of bulk rock, was measured at the Nordic Center for Earth Evolution

at the University of Southern Denmark, Odense, on Ag2S precipitates from 22 samples of the

sulphide that was liberated by the CRS method (Newton et al., 1995; Lyons, 1997). About

200 g were added to a tin cup with V2O5 and combusted using a Thermo elemental analyzer

coupled via a Conflow III interface to a Thermo Delta V Plus mass spectrometer. Sulphur

isotope compositions are expressed as permil () deviations from V-CDT using the

conventional delta notation (Fig. S17) with a standard deviation of about 0.2.



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Figure S17 |34S values ( V-CDT) measured on 22 samples from the lower (FB1) and theupper (FB2) parts of the Francevillian B Formation.

Iron

Iron speciation was investigated using the sequential extraction protocol (Poulton &

Canfield, 2005) and sulphide concentrations were determined by the chromium reduction

method (CRS) (Zhabina & Volkov, 1978; Canfield et al., 1986). The concentration of iron in

all iron fractions, except for pyrite, were measured by atomic absorption spectrometry (AAS),

while pyrite content was estimated from the sulphide concentrations by Cr reduction

assuming a pyrite stoichiometry (Fe2S) in the sediment. Reproducibility was above 95% for

all phases but magnetite (Femag), where concentrations were close to zero and we consider the

error to be within the detection level of the AAS.

The highly reactive iron (FeHR) is considered to be the diagenetically active iron and is

defined as the sum of carbonate-associated iron (Fecarb), ferric oxides (Feox) and Femag, plus all

the iron that has been converted to sulphide phases in the water column or sediment (Fepy)

(Canfield et al., 1992; Poulton et al., 2004); so FeHR= Fecarb + Feox + Femag + Fepy. The highly

reactive iron is then related to total iron content of the sediment (FeT) to form a redox

indicator, as sediments deposited below an anoxic water column usually have a FeHR/FeT ratio

above 0.38 (Raiswell & Canfield, 1998; Poulton & Raiswell, 2002; Canfield et al., 2008). We

applied this iron speciation technique to 24 well-preserved rock samples. In our dataset there

are four samples with FeHR/FeT >0.38, indicating anoxia, while the other 20 samples are

consistent with oxygenated water-column conditions (Fig. S18). The analyzed samples were



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not deposited by turbidities, which could distort an anoxic iron signal (Raiswell & Canfield,

1998), thus we interpret this sample set to have been deposited in a predominantly oxic

environment.

FeHR/FeT

0,00

0,10

0,20

0,30

0,40

0,50

0,60

0,70

FB2 FB1

Figure S18 | Ratio of highly reactive to total Fe (FeHR/FeT) measured in 24 samples from thelower (FB1) and the upper (FB2) units of the Francevillian B Formation.



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Movie 1 | Specimen G-FB2-f mst1.1.Movie 2 | Specimen G-FB2-f mst2.1.Movie 3 | Specimen G-FB2-f mst3.1.Movie 4 | Specimen G-FB2-f mst4.1.

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