Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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


The evidence for macroscopic life during the Palaeoproterozoic era (2.5–1.6 Gyr ago) is controversial1,2,3,4,5. Except for the nearly 2-Gyr–old coil-shaped fossil Grypania spiralis6,7, which may have been eukaryotic, evidence for morphological and taxonomic biodiversification of macroorganisms only occurs towards the beginning of the Mesoproterozoic era (1.6–1.0 Gyr)8. Here we report the discovery of centimetre-sized structures from the 2.1-Gyr-old black shales of the Palaeoproterozoic Francevillian B Formation in Gabon, which we interpret as highly organized and spatially discrete populations of colonial organisms. The structures are up to 12 cm in size and have characteristic shapes, with a simple but distinct ground pattern of flexible sheets and, usually, a permeating radial fabric. Geochemical analyses suggest that the sediments were deposited under an oxygenated water column. Carbon and sulphur isotopic data indicate that the structures were distinct biogenic objects, fossilized by pyritization early in the formation of the rock. The growth patterns deduced from the fossil morphologies suggest that the organisms showed cell-to-cell signalling and coordinated responses, as is commonly associated with multicellular organization9. The Gabon fossils, occurring after the 2.45–2.32-Gyr increase in atmospheric oxygen concentration10, may be seen as ancient representatives of multicellular life, which expanded so rapidly 1.5 Gyr later, in the Cambrian explosion.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: Simplified geological map of Gabon.
Figure 2: Examples of black shale bedding surfaces.
Figure 3: In situ macrofossil specimen from the FB2 Formation.
Figure 4: Micro-CT-based reconstructions and virtual sections of four specimens from the FB2 macrofossil record of Gabon.
Figure 5: Section through specimen G-FB2-f-mst4.3.


  1. Seilacher, A., Bose, P. K. & Pflüger, F. Triploblastic animals more than 1 billion years ago: trace fossil evidence from India. Science 282, 80–83 (1998)

    Article  ADS  CAS  Google Scholar 

  2. Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Philos. Trans. R. Soc. London B 361, 1023–1038 (2006)

    Article  CAS  Google Scholar 

  3. Bengtson, S., Rasmussen, B. & Krapež, B. The Paleoproterozoic megascopic Stirling biota. Paleobiology 33, 351–381 (2007)

    Article  Google Scholar 

  4. Lamb, D. M., Awramik, S. M. & Zhu, S. Paleoproterozoic compression-like structures from the Changzhougou Formation, China: eukaryotes or clasts? Precambr. Res. 154, 236–247 (2007)

    Article  ADS  CAS  Google Scholar 

  5. Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1105 (2008)

    Article  ADS  CAS  Google Scholar 

  6. Han, T.-M. & Runnegar, B. Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee Iron-Formation, Michigan. Science 257, 232–235 (1992)

    Article  ADS  CAS  Google Scholar 

  7. Schneider, D. A., Bickford, M. E., Cannon, W. F., Schulz, K. J. & Hamilton, M. A. Age of volcanic rocks and syndepositional iron formations, Marquette Range Supergroup: implications for the tectonic setting of Paleoproterozoic iron formations of the Lake Superior region. Can. J. Earth Sci. 39, 999–1012 (2002)

    Article  ADS  CAS  Google Scholar 

  8. Bengtson, S., Belivanova, V., Rasmussen, B. & Whitehouse, M. The controversial “Cambrian” fossils of the Vindhyan are real but more than a billion years older. Proc. Natl Acad. Sci. USA 106, 7729–7734 (2009)

    Article  ADS  CAS  Google Scholar 

  9. Shapiro, J. A. & Dworkin, M. (eds) Bacteria as Multicellular Organisms (Oxford Univ. Press, 1997)

    Google Scholar 

  10. Bekker, A. et al. Dating the rise of atmospheric oxygen. Nature 427, 117–120 (2004)

    Article  ADS  CAS  Google Scholar 

  11. Gauthier-Lafaye, F. & Weber, F. The Francevillian (Palaeoproterozoic) uranium ore deposits of Gabon. Chem. Geol. 84, 2267–2285 (1989)

    CAS  Google Scholar 

  12. Gauthier-Lafaye, F. & Weber, F. Natural nuclear fission reactors: time constraints for occurrence, and their relation to uranium and manganese deposits and to the evolution of the atmosphere. Precambr. Res. 120, 81–100 (2003)

    Article  ADS  CAS  Google Scholar 

  13. Bros, R., Stille, P., Gauthier-Lafaye, F., Weber, F. & Clauer, N. Sm-Nd isotopic dating of Proterozoic clay material: an example from the Francevillian sedimentary series, Gabon. Earth Planet. Sci. Lett. 113, 207–218 (1992)

    Article  ADS  CAS  Google Scholar 

  14. Hoori, K., Hidaka, H. & Gauthier-Lafaye, F. U-Pb geochronology and geochemistry of zircon from the Franceville series at Bidoudouma, Gabon. The 15th Annual Goldschmidt Conference. (2005)

  15. Gancarz, A. J. in The Natural Fission Reactors: Annual International Atomic Energy Agency Conference 513–520 (TC-119/40, IAEA, 1978)

    Google Scholar 

  16. Bekker, A. et al. Fractionation between inorganic and organic carbon during the Lomagundi (2.22–2.1 Ga) carbon isotope excursion. Earth Planet. Sci. Lett. 271, 278–291 (2008)

    Article  ADS  CAS  Google Scholar 

  17. Habicht, K. S., Gade, M., Thamdrup, B., Berg, P. & Canfield, D. E. Calibration of sulfate levels in the Archean ocean. Science 298, 2372–2374 (2002)

    Article  ADS  CAS  Google Scholar 

  18. Farrell, Ú. C., Martin, M. J., Hagadorn, J. W., Whiteley, T. & Briggs, D. E. G. Beyond Beecher’s Trilobite Bed: widespread pyritization of soft tissues in the Late Ordovician Taconic foreland basin. Geology 37, 907–910 (2009)

    Article  ADS  Google Scholar 

  19. Seilacher, A., Buatois, L. & Mángano, M. G. Trace fossils in the Ediacaran–Cambrian transition: behavioral diversification, ecological turnover and environmental shift. Palaeogeogr. Palaeoclimatol. Palaeoecol. 227, 323–356 (2005)

    Article  Google Scholar 

  20. Wacey, D. Early Life on Earth: A Practical Guide (Springer, 2009)

    Book  Google Scholar 

  21. Cortial, F., Gauthier-Lafaye, F., Lacrampe-Couloume, G., Oberlin, A. & Weber, F. Characterization of organic matter associated with uranium deposits in the Francevillian formation of Gabon (lower proterozoic). Org. Geochem. 15, 73–85 (1990)

    Article  CAS  Google Scholar 

  22. Mossman, D. J., Gauthier-Lafaye, F. & Jackson, S. Carbonaceous substances associated with the Paleoproterozoic natural nuclear fission reactors of Oklo, Gabon: paragenesis, thermal maturation and carbon isotopic and trace element composition. Precambr. Res. 106, 135–148 (2001)

    Article  ADS  CAS  Google Scholar 

  23. Dutkiewicz, A., George, S. C., Mossman, D. J., Ridley, J. & Volk, H. Oil and its biomarkers associated with the Palaeoproterozoic Oklo natural fission reactors, Gabon. Chem. Geol. 244, 130–154 (2007)

    Article  ADS  CAS  Google Scholar 

  24. Ben-Jacob, E. Bacterial self-organization: co-enhancement of complexification and adaptability in a dynamic environment. Philos. Transact. Ser. A 361, 1283–1312 (2003)

    Article  ADS  MathSciNet  Google Scholar 

  25. Grazhdankin, D. & Gerdes, G. Ediacaran microbial colonies. Lethaia 40, 201–210 (2007)

    Article  Google Scholar 

  26. Allwood, A. C., Walter, M. R., Kamber, B. S., Marshall, C. P. & Burch, I. W. Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714–718 (2006)

    Article  ADS  CAS  Google Scholar 

  27. Schieber, J. in Atlas of Microbial Mat Features Preserved within the Clastic Rock Record (eds Schieber, J. et al.) 117–134 (Elsevier, 2007)

    Google Scholar 

  28. Bonner, J. T. First Signals: The Evolution of Development (Princeton Univ. Press, 2000)

    Google Scholar 

  29. Canfield, D. E. et al. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321, 949–952 (2008)

    Article  ADS  CAS  Google Scholar 

  30. Frei, R., Gaucher, C., Poulton, S. W. & Canfield, D. E. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461, 250–254 (2009)

    Article  ADS  CAS  Google Scholar 

Download references


We thank the Ministry of Mines, Oil, Energy and Hydraulic Resources and the General Direction of Mines and Geology of Gabon for collaboration and assistance, and the French Embassy at Libreville and the French Ministry for Foreign Affairs for support. We thank F. Mayaga-Mikolo, D. Beaufort, B. Cost, D. Thieblemont, F. Pambo and H. Sigmund for discussions. For assistance in Gabon 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 Institut Français du Pétrole, the Swiss Light Source (TOMCAT beamline) at the Paul Scherrer Institute, and the Centre de Microtomographie at the University of Poitiers (CdMT). Nordsim is operated under an agreement of the Joint Committee of the Nordic Research Councils for Natural Sciences (NOS-N), with further funding from the Knut and Alice Wallenberg Foundation; this is Nordsim contribution 256. Research was supported by the French CNRS-INSU, the Bureau de Recherches Géologiques et Minières (BRGM), the Danish National Research Foundation and the Swedish Research Council.

Author information

Authors and Affiliations



A.E.A. conceived and headed the project. 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. and A.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.Meunier analysed data. A.E.A., S.B., D.E.C., R.M. and E.H. wrote the main part of the 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., A.R., D.V., M.W. and A.Meunier provided critical input to the manuscript.

Corresponding author

Correspondence to Abderrazak El Albani.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

The repository of the fossils is the Department of Geosciences, University of Poitiers, France.

Supplementary information

Supplementary Information

This file contains Supplementary Information and Data 1-6, Supplementary Figures S1-S18 with legends, Supplementary Tables S1-S5 and References. (PDF 2816 kb)

Supplementary Movie 1

This file contains an animation of G-FB2-f mst1.1 microtomographic reconstruction showing inner structures through transparency. (MPG 8301 kb)

Supplementary Movie 2

This file contains an animation of G-FB2-f mst2.1 microtomographic reconstruction showing inner structures through transparency. (MPG 12465 kb)

Supplementary Movie 3

This file contains an animation of G-FB2-f mst3.1 microtomographic reconstruction showing inner structures through transparency. (MPG 9651 kb)

Supplementary Movie 4

This file contains an animation of G-FB2-f mst4.1 microtomographic reconstruction showing inner structures through transparency. (MPG 9190 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Albani, A., Bengtson, S., Canfield, D. et al. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466, 100–104 (2010).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing