Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago

37 Pages·2010·3.57 MB·English

by  Abderrazak El Albani

Vol466|1July2010|doi:10.1038/nature09166
LETTERS
Large colonial organisms with coordinated growth in
oxygenated environments 2.1 Gyr ago
AbderrazakElAlbani1,StefanBengtson2,DonaldE.Canfield3,AndreyBekker4,RobertoMacchiarelli5,6,
ArnaudMazurier7,EmmaU.Hammarlund2,3,8,PhilippeBoulvais9,Jean-JacquesDupuy10,ClaudeFontaine1,
FranzT.Fu¨rsich11,Franc¸oisGauthier-Lafaye12,PhilippeJanvier13,EmmanuelleJavaux14,FrantzOssaOssa1,
Anne-CatherinePierson-Wickmann9,ArmelleRiboulleau15,PaulSardini1,DanielVachard15,MartinWhitehouse16
&AlainMeunier1
The evidence for macroscopic life during the Palaeoproterozoic intercalatedvolcanicandcontinentalsedimentsaccumulatedduring
era (2.5–1.6Gyr ago) is controversial1–5. Except for the nearly theultimatefillingphaseofthebasin(SupplementaryFig.1).
2-Gyr–oldcoil-shapedfossilGrypaniaspiralis6,7,whichmayhave
beeneukaryotic,evidenceformorphologicalandtaxonomicbio-
diversificationofmacroorganismsonlyoccurstowardsthebegin-
ningoftheMesoproterozoicera(1.6–1.0Gyr)8.Herewereportthe
discovery of centimetre-sized structures from the 2.1-Gyr-old
blackshalesofthePalaeoproterozoicFrancevillian BFormation Gabon
in Gabon, which we interpret as highly organized and spatially
discrete populations of colonial organisms. The structures are
upto12cminsizeandhavecharacteristicshapes,withasimple
butdistinctgroundpatternofflexiblesheetsand,usually,aper-
meatingradialfabric.Geochemicalanalysessuggestthatthesedi- Volcanic complex of N’Goutou
mentsweredepositedunderanoxygenatedwatercolumn.Carbon
andsulphurisotopicdataindicatethatthestructuresweredistinct
Okondja
biogenicobjects,fossilizedbypyritizationearlyintheformation Basin
oftherock.Thegrowthpatternsdeducedfromthefossilmorpho-
Plateau des
logies suggest that the organisms showed cell-to-cell signalling
Abeilles
andcoordinatedresponses,asiscommonlyassociatedwithmulti-
cellular organization9. The Gabon fossils, occurring after the Lastoursville
Basin
2.45–2.32-Gyr increase in atmospheric oxygen concentration10,
maybeseenasancientrepresentativesofmulticellularlife,which Ondili shoal
expandedsorapidly1.5Gyrlater,intheCambrianexplosion. Francevillian
Basin
OursamplescomefromtheFrancevillianGroup,whichbelongsto
Archean basement
a well-recognized lithostratigraphic succession, outcropping across
35,000km2insoutheasternGabon11,12.Thisgroupisexposedinthe
intracratonic basins of Plateau des Abeilles, Lastoursville and Franceville
0 50 km
Franceville (Fig. 1), and reaches a maximum thickness of about
2,000m.
The group consists of five unmetamorphosed and undeformed
sedimentary formations, FA to FE, bounded by conformable sur-
faces11,12.Thelowerpartofthesequence(FAFormation)comprises Volcanic rocks of N’Goutou Gneiss of Okanja
fluvialdepositsofalow-standsystemtractdominatedbyonshore-to-
Phanaerozoic deposit Gneiss of Ogoue
coastalsandstones.IntheFBFormation,marinedeltaicdepositionis
indicatedbyfaciesdevelopmentandsedimentarystructuressuchas Francevillian group Gneiss and granite (Archaean)
load casts, water escape structures, cross-stratification and hum- Figure1|SimplifiedgeologicalmapofGabon. ShowingtheFrancevillian
mockycross-stratification.Shallowerwaterconditionsareobserved basin(inset)andthelocationofthefossiliferoussite(star)nearthetownof
intheFCFormation,whereassubsequentdeposits(FDandFE)show Franceville.
1LaboratoireHYDRASA,UMR6269CNRS-INSU,Universite´dePoitiers,86022Poitiers,France.2DepartmentofPalaeozoology,SwedishMuseumofNaturalHistory,Box50007,SE-
10405Stockholm,Sweden.3NordicCenterforEarthEvolution,DK-5230OdenseM,Denmark.4DepartmentofGeologicalSciences,UniversityofManitoba,Manitoba,R3T2N2
Canada.5De´partementGe´osciences,CentredeMicrotomographie,Universite´dePoitiers,86022Poitiers,France.6De´partementdePre´histoire,UMR7194CNRS,Muse´umNational
d’HistoireNaturelle,Paris,75005,France.7Socie´te´EtudesRecherchesMate´riaux,CRIBiopole,86000Poitiers,France.8DepartmentofGeologicalSciences,StockholmUniversity,SE-
10691Stockholm,Sweden.9De´partementGe´osciences,UMR6118,Universite´deRennes,35042Rennes,France.10BureaudeRecherchesGe´ologiquesetMinie`res,45060Orle´ans,
France.11GeoZentrumNordbayern,Universita¨tErlangen,FachgruppePala¨oumwelt,D91054Erlangen,Germany.12Laboratoired’HydrologieetdeGe´ochimiedeStrasbourg,UMR7517
CNRS,67084Strasbourg,France.13De´partementHistoiredelaTerre,UMR7207CNRS,Muse´umNationald’HistoireNaturelle,Paris,75005,France.14De´partementdeGe´ologie,
Unite´deRecherchePale´obotanique-Pale´opalynologie-Micropale´ontologie,Universite´deLie`ge,Sart-TilmanLie`ge4000,Belgium.15LaboratoireGe´osyste`mes,FRE3298CNRS,
Universite´Lille1,59655Villeneuved’Ascq,France.16LaboratoryforIsotopeGeology,SwedishMuseumofNaturalHistory,Box50007,SE-10405Stockholm,Sweden.
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NATURE|Vol466|1July2010 LETTERS
ThelowerpartoftheinvestigatedFB2section,whereFB2isthe a
upperpartofFB,outcroppingnearFranceville,consistsofsandstone
beds deposited in channels near the fair-weather wave base in the
low-energyenvironmentofaprogradingdelta.Thetopmostpartof
this section consists of an oxidized and stromatolitic hardground
surface. This is sharply overlain by a 5-m-thick deposit of finely
laminated horizontal black shales, interbedded with thin siltstone
layers, deposited by waning storm surge without any evidence for
subaerialexposure(SupplementaryFig.1).TheageoftheFBdeposits
is well constrained to 2,100630Myr (refs 13–15), roughly con-
temporaneouswiththe,2.22–2.10GyrLomagundimarinepositive
carbon-isotope excursion16 (see Supplementary Information and
SupplementaryFig.1)andabout200–250Myrafterthefirstsignifi-
cantriseinatmosphericoxygenconcentration10.
Morethan250pyritizedspecimensembeddedwithintheirsedi-
mentarymatrixwerecollectedinsitufromatleast18thinhorizons,
identified within the FB2 black shale lithofacies (Supplementary
b
Fig. 2). In some cases, the layers containing the specimens were
locallycoatedwithironoxides,owingtooxidationofpyritecrystals.
Thespecimensrangeinshapefromelongatedtonearlyisodiametric
forms,withoccasionalfinger-likeprotrusions(Fig.2,Supplementary
Fig.3).Theirlengthandwidthrangefrom7to120mmandfrom,5
to70mmrespectively,andtheirthicknessvariesfrom,1to10mm.
Weestimateadensityofupto40specimensperm2,withformsof
different sizes and shapes and disparate orientations occurring c
together(SupplementaryFigs3,4).
Weusedmicro-computedtomography(micro-CT)-basedthree-
dimensional (3D) imaging to characterize the outer and inner
morphologies of the structures (see Supplementary Information).
Mostspecimensshowapatternofradialfabricattheouteredgeof
Figure3|InsitumacrofossilspecimenfromtheFB2Formation. a,Lower
their undulate or lobate periphery (Figs 2, 3, 4a–c, Supplementary
sideofthefossil(top)withitsimpressionleftintheblackshales(bottom),
Figs5–8);thisisoftencurved,soastomeettheouterrimataroughly showingperipheralradialfabricandwrinkledappearance.b,Micro-CT-
perpendicularangle.Insomecases,theradialfabricdoesnotreach basedvirtualreconstruction(volumerenderedinsemi-transparency),
theouterrim(Fig.4d),whereasinothersitissimplylacking.The showingradialfabricandtwoinnerpyriteconcretions.c,Longitudinal
centralpartsofthelargerformsarecommonlythrownintosmooth, virtualsectionrunningclosetotheestimatedcentralpartofthespecimen,
transverse folds, which do not reach the outer edge and which are evidencingthefoldpattern.Scalebars,1.0cm.
externally expressed as wrinkling of the structure (Figs 3, 4b–c,
SupplementaryFig.6–8,11).Laminaeofthehostshalearedraped
aroundthefolds(SupplementaryFig.13),showingthatthefolding
a
occurred before compaction. X-ray diffraction analyses show no
mineralogicaldifferencebetweentheclaymatricesinthespecimens
andthehostshale(SupplementaryFig.14,SupplementaryTable1).
Thelargerspecimensoftenalsocontainacentralpyritebody(Figs3,
4c, d, Supplementary Figs 8, 11), which is developed differently.
Sometimes it forms a median layer within the folded sheet (Sup-
plementary Figs 6–8), but it is more often nodular (Figs 3b, 4c–d,
Supplementary Figs 8, 11), sometimes deflecting the transverse
folds (Fig. 4c, Supplementary Fig. 11). We measured topographic
thickness along geometrically homologous virtual sections, which
indicated progressive thinning towards the periphery (Supplemen-
taryFigs9,10).
b DifferencesinX-rayattenuationwithin the specimensare largely
duetothedifferentialdistributionofoctahedralpyritecrystals.The
peripheralradialfabricischaracterizedbypyrite-freeregionsexpressed
in the microfabric as canals or slits (Supplementary Figs 12, 15).
Secondary-ionizationmass-spectrometricanalysisofthepyritereveals
verylightd34Svaluesofabout225%to230%inthefossilizedsheets,
withthecentralpyritenoduletendingtowardsheaviervaluesof5%to
15%,particularlyintheoutermargins(Fig.5,SupplementaryTable2).
Thesheet,whichrepresentsthemainbodyofthefossilizedstructure,
wasthereforepyritizedduringearlydiagenesis,whensulphatereducers
wereindirectcontactwiththeeffectivelyunlimitedsulphatepoolof
theoverlyingwatercolumn.Thehighfractionationssuggestsulphate
concentrationsinexcessof200mM(ref.17)(SupplementaryFig.17).
Figure2|Examplesofblackshalebeddingsurfaces. a,b,Bearing Thepyritizednodulesapparentlyformedlater,fromporefluidsmore
macrofossilsincolonyformfromtheFB2level.Scalebars,1.0cm. depletedinsulphate,andthepatternofsulphurisotopessuggeststhat
101
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LETTERS NATURE|Vol466|1July2010
a b c d
a b c d
15
a b c d
δ34S
a b c d 1 mm
–30
Figure4|Micro-CT-basedreconstructionsandvirtualsectionsoffour Figure5|SectionthroughspecimenG-FB2-f-mst4.3. d34Svalues
specimensfromtheFB2macrofossilrecordofGabon. Samplesshowa
(colouredspots,seescale)aremeasuredinthecentralpyritenodule(centre)
disparityofformsbasedon:externalsizeandshapecharacteristics;
andsurroundingsheetmaterial(topandbottom)bysecondary-ionization
peripheralradialmicrofabric(missinginviewd);patternsoftopographic
massspectrometry.SeeSupplementaryInformation.
thicknessdistribution;generalinnerstructuralorganization,including
occurrenceoffolds(seeninviewsbandc)andofanodularpyriteconcretion patternoftheGabonfossils,andthereisnostructuralevidenceof
inthecentralpartofthefossil(absentinviewsaandb).a,Original sedimentinjectioninassociationwiththefossils.TheGabonfossils
specimen.b,Volumerenderinginsemi-transparency.c,Transverse(axial) alsoresembleradiallygrowingpyriteormarcasitecrystals,or‘pyrite
two-dimensionalsection.d,Longitudinalsectionrunningclosetothe
suns’,whichareoccasionallyfoundinPhanaerozoicshales.However,
estimatedcentralpartofthespecimen.Scalebars,5mm.Specimensfrom
amicro-CT-basedcomparisonoftheinnerstructuresclearlyshows
toptobottom:G-FB2-f-mst1.1,G-FB2-f-mst2.1,G-FB2-f-mst3.1,G-FB2-f-
that the ‘pyrite suns’ have a much more regular and linear radial
mst4.1.
fabric than the Gabon specimens, and that this fabric extends all
pyritizationbeganatthecentreandcontinuedtowardstheoutermar- thewaytothecentreofthestructure,withoutanyevidenceofflexible
gins, duringwhichprocesstheremainingsulphate became progres- folding (Supplementary Fig. 16). Indeed, we are unaware of any
sivelymore depletedinlight isotopes.The sulphur isotopepatterns inorganic processes that can generate the style of flexible folding
thussupporttheinterpretationthatthepyritizedsheetsrepresentearly andirregularradialfabricthatweobserveintheGabonfossils(Fig.4).
diagenesisoforiginalbiologicalfabric,whereastheoccasionalcentral Theaccumulatedevidencesuggeststhatthestructuresarebiogenic.
lumpofpyriteisalater,post-burial,diageneticfeaturethatisnotlikely Thefoldpatternseeninthecentreofmostofthespecimensindicates
toreflectoriginalmorphology. deformationofaflexiblesheet,implyinganoriginallycohesivestruc-
The differences in the organic carbon d13C content recorded tureoforganiccomposition.Theradialfabriciscommonlydeflected
betweenfivespecimensandtheirassociatedhostshalesedimentalso tomeettherimofthespecimen,suggestingthattheoriginalmaterial
supportthefossilizedstructuresrepresentingadistinctorganicentity wasgrowing byperipheralaccretionofflexible organic matter. We
(SupplementaryTable3).Plantsandbiomineralizedanimaltissues concludethattheGabonstructuresfulfilthegeneralcriteriaofbio-
ofthePhanaerozoiceonarecommonlypyritized;pyritizationofsoft genicity applied to fossil-like forms in the early rock record20
tissuesisrarebuttypicallyresultsinfaithfulreplication.Thispreser- (SupplementaryTable4).Thepresenceofabundantorganicmatter
vationisthoughttobefavouredbyalowcontentoforganicmole- intheFBFormation21,22(SupplementaryTable5),includingsteranes
culesandhighcontentofreactiveironinthepore-waters18. ofeukaryoticorigin23,isconsistentwiththisinterpretation.
Wefindnoevidencetosupportaninorganicoriginofthestruc- Weconsideritmostlikelythatthesestructuresrepresentfossilized
turesfromtheFB2blackshalelevel,whetherconcretionsresulting colonialorganisms.Bacterialcoloniesgrowingonsurfacesareknown
from epitaxic/crystal growth processes, or features of diagenetic, tocoordinatetheirbehaviour,resultinginregularshapesanddistinct
sedimentary,hydrothermal,ortectonicorigin.Thereisasuperficial fabrics9; radial fabrics are common, and are thought to be due to
resemblancebetweentheGabonstructuresandtheEdiacarandubio- repulsivechemotaxis24.Moststudiesofbacterialcolonygrowthhave
fossilMawsonitesspriggi,whichhasbeeninterpretedasasandvol- beendoneonmonocultures inPetridishes,wherecoloniesexceed
cano interacting with biomats19; however, this interpretation centimetre size9. In nature, ‘fairy-ring’ colonies, formed by cyano-
accountsforneitherthefineinternalradialfabricnortheinnerfold bacteriaanddiatomsandreachingadiameter of15cm,havebeen
102
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NATURE|Vol466|1July2010 LETTERS
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Received29March;accepted4May2010. AcknowledgementsWethanktheMinistryofMines,Oil,EnergyandHydraulic
ResourcesandtheGeneralDirectionofMinesandGeologyofGabonfor
1. Seilacher,A.,Bose,P.K.&Pflu¨ger,F.Triploblasticanimalsmorethan1billionyears collaborationandassistance,andtheFrenchEmbassyatLibrevilleandtheFrench
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Stirlingbiota.Paleobiology33,351–381(2007). Parneix,D.Proust,M.StampanoniandX.Valentin.Wealsoacknowledgethe
103
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LETTERS NATURE|Vol466|1July2010
InstitutFranc¸aisduPe´trole,theSwissLightSource(TOMCATbeamline)atthe A.E.A.,C.F.,F.O.O.andA.Meunieranalysedmineralogy.S.B.,D.E.C.,A.B.,E.H.,P.B.,
PaulScherrerInstitute,andtheCentredeMicrotomographieattheUniversityof A.-C.P.-W.,A.R.andM.W.carriedoutisotopeandgeochemicalanalyses.F.G.-L.
Poitiers(CdMT).NordsimisoperatedunderanagreementoftheJointCommittee providedgeologicalsamples.A.E.A.,S.B.,D.E.C.,A.B.,R.M.,A.Mazurier,E.H.,P.B.,
oftheNordicResearchCouncilsforNaturalSciences(NOS-N),withfurther 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.andA.Meunier
fundingfromtheKnutandAliceWallenbergFoundation;thisisNordsim analyseddata.A.E.A.,S.B.,D.E.C.,R.M.andE.H.wrotethemainpartofthe
contribution256.ResearchwassupportedbytheFrenchCNRS-INSU,theBureau manuscript.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.,
deRecherchesGe´ologiquesetMinie`res(BRGM),theDanishNationalResearch A.R.,D.V.,M.W.andA.Meunierprovidedcriticalinputtothemanuscript.
FoundationandtheSwedishResearchCouncil.
AuthorInformationTherepositoryofthefossilsistheDepartmentof
AuthorContributionsA.E.A.conceivedandheadedtheproject.A.E.A.,S.B.,D.E.C., Geosciences,UniversityofPoitiers,France.Reprintsandpermissionsinformation
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©2010Macmillan Publishers Limited. All rights reserved
doi: 10.1038/nature09166
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1 - The Francevillian Group and the FB2 section

Figure S1 | a, Lithostratigraphy of the Palaeoproterozoic Francevillian group with the five
Formations (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 δ13C values and of total organic carbon (TOC, wt. %)
carb
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 δ13C 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 level
photographed 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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