Letter | Published:

Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia

Nature Geoscience volume 4, pages 698702 (2011) | Download Citation



Sulphur isotope data from early Archaean rocks suggest that microbes with metabolisms based on sulphur existed almost 3.5 billion years ago, leading to suggestions that the earliest microbial ecosystems were sulphur-based1,2,3,4,5. However, morphological evidence for these sulphur-metabolizing bacteria has been elusive. Here we report the presence of microstructures from the 3.4-billion-year-old Strelley Pool Formation in Western Australia that are associated with micrometre-sized pyrite crystals. The microstructures we identify exhibit indicators of biological affinity, including hollow cell lumens, carbonaceous cell walls enriched in nitrogen, taphonomic degradation, organization into chains and clusters, and δ13C values of −33 to −46‰ Vienna PeeDee Belemnite (VPDB). We therefore identify them as microfossils of spheroidal and ellipsoidal cells and tubular sheaths demonstrating the organization of multiple cells. The associated pyrite crystals have Δ33S values between −1.65 and +1.43‰ and δ34S values ranging from −12 to +6‰ Vienna Canyon Diablo Troilite (VCDT)5. We interpret the pyrite crystals as the metabolic by-products of these cells, which would have employed sulphate-reduction and sulphur-disproportionation pathways. These microfossils are about 200 million years older than previously described6 microfossils from Palaeoarchaean siliciclastic environments.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

    , & Isotopic evidence for microbial sulphate reduction in the early Archean era. Nature 410, 77–81 (2001).

  2. 2.

    et al. Early Archaean microorganisms preferred elemental sulfur, not sulfate. Science 317, 1534–1537 (2007).

  3. 3.

    , , & Quadruple sulfur isotope analysis of ca. 3.5 Ga Dresser Formation: New evidence for microbial sulfate reduction in the early Archean. Geochim. Cosmochim. Acta 72, 5675–5691 (2008).

  4. 4.

    , , , & Evaluating the role of microbial sulfate reduction in the early Archean using quadruple isotope systematics. Earth Planet. Sci. Lett. 279, 383–391 (2009).

  5. 5.

    , , & Two coexisting sulfur metabolisms in a ca. 3400 Ma sandstone. Geology 38, 1115–1118 (2010).

  6. 6.

    , & Organic-walled microfossils in 3.2 billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934–938 (2010).

  7. 7.

    Microfossils of the Early Archean Apex Chert: New evidence for the antiquity of life. Science 260, 640–646 (1993).

  8. 8.

    et al. Questioning the evidence for Earth’s oldest fossils. Nature 416, 76–81 (2002).

  9. 9.

    & Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431, 549–552 (2004).

  10. 10.

    & Hydrogen-based carbon fixation in the earliest known photosynthetic organisms. Geology 34, 37–40 (2006).

  11. 11.

    , , , & Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714–718 (2006).

  12. 12.

    Regional review of the 3426–3350 Ma Strelley Pool Formation, Pilbara Craton, Western Australia. Geol. Surv. W.A. Rec 2008/15, 27 (Geological Survey of Western Australia, 2008).

  13. 13.

    et al. Record of emergent continental crust 3.5 billion years ago in the Pilbara Craton of Australia. Nature 375, 574–577 (1995).

  14. 14.

    et al. The 3.4 billion-year-old Strelley Pool sandstone: A new window into early life on Earth. Int. J. Astrobiol. 5, 333–342 (2006).

  15. 15.

    , & Geological and trace element evidence for a marine sedimentary environment of deposition and biogenicity of 3.45 Ga stromatolitic carbonates in the Pilbara Craton, and support for a reducing Archean ocean. Geobiology 1, 91–108 (2003).

  16. 16.

    Sedimentary Petrology 3rd edn 263 (Blackwell Science, 2001).

  17. 17.

    et al. Biogenicity of morphologically diverse carbonaceous microstructures from the ca. 3400 Ma Strelley Pool Formation, in the Pilbara Craton. West. Aust. Astrobiol. 10, 899–920 (2010).

  18. 18.

    , & Thermal history of the 3.5–3.2 Ga Onverwacht and Fig Tree Groups, Barberton greenstone belt, South Africa, inferred by Raman microspectroscopy of carbonaceous material. Geology 32, 37–40 (2004).

  19. 19.

    Crystal Structures 2nd edn, Vol. 1 (Wiley, 1963).

  20. 20.

    Geology of the North Shaw 1:100,000 sheet: Geol. Surv. W.A. Geol. Series Explan. Notes 86 (Geological Survey of Western Australia, 2000).

  21. 21.

    Early silica cementation and subsequent diagenesis in arenites from four early Proterozoic iron formations of North America. J. Sedim. Res. 57, 494–511 (1987).

  22. 22.

    & A transmission electron microscopy study of silica and kerogen biosignatures in 1.9 Ga Gunflint microfossils. Astrobiology 4, 196–210 (2004).

  23. 23.

    in The Precambrian Earth: Tempos and Events (eds Eriksson, P. G., Altermann, W., Nelson, D. R., Mueller, W. U. & Catuneanu, O.) 516–539 (Elsevier, 2004).

  24. 24.

    Fossil evidence of Archaean life. Phil. Trans. R. Soc. B 361, 869–885 (2006).

  25. 25.

    , , & A fresh look at the fossil evidence for early Archaean cellular life. Phil. Trans. R. Soc. B 361, 887–902 (2006).

  26. 26.

    Microbial Mats in Sandy Deposits from the Archean Era to Today 194 (Springer, 2010).

  27. 27.

    A 3,800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333, 313–318 (1988).

  28. 28.

    , , & Earliest microbially mediated pyrite oxidation in 3.4 billion-year-old sediments. Earth Planet. Sci. Lett. 301, 393–402 (2011).

  29. 29.

    , , & Sulfur isotope effects in the disproportionation reaction of sulfur dioxide in hydrothermal fluids: Implications for the δ34S variations of dissolved bisulfate and elemental sulfur from active crater lakes. J. Volcanol. Geotherm. Res. 97, 287–307 (2000).

  30. 30.

    , & Ultrastructure, aggregation-state, and crystal growth of biogenic nanocrystalline sphalerite and wurtzite. Am. Mineral. 89, 950–960 (2004).

Download references


The authors acknowledge the facilities, scientific and technical assistance of the AMMRF at both the Centre for Microscopy Characterization and Analysis, The University of Western Australia, and Adelaide Microscopy, The University of Adelaide. These facilities are funded by the Universities, State and Commonwealth Governments. The Geological Survey of Western Australia, C. Stoakes, N. McLoughlin and O. Green are thanked for assistance with fieldwork, A. Steele for providing access to laser Raman facilities, and S. Menon and L. Green for assistance with FIB sample preparation. D.W. is supported by a postdoctoral fellowship from The University of Western Australia. M.D.B. and D.W. were funded for the initial stages of this research by a NERC grant to M.D.B. (NE/C510883/1) and by the support of the University of Oxford.

Author information


  1. Centre for Microscopy, Characterization and Analysis, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia

    • David Wacey
    • , Matt R. Kilburn
    • , Martin Saunders
    •  & John Cliff
  2. School of Earth and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009, Australia

    • David Wacey
  3. Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK

    • Martin D. Brasier


  1. Search for David Wacey in:

  2. Search for Matt R. Kilburn in:

  3. Search for Martin Saunders in:

  4. Search for John Cliff in:

  5. Search for Martin D. Brasier in:


D.W., M.R.K. and M.D.B. performed the field mapping and collected samples. M.D.B. and D.W. carried out the petrography. M.R.K. and D.W. performed the NanoSIMS analyses. J.C. performed the IMS 1280 carbon isotope analyses. M.S. performed the TEM analyses. D.W. performed the sample preparation and some of the FIB-SEM work. All authors helped to interpret the data. D.W. and M.D.B. wrote the paper. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to David Wacey or Matt R. Kilburn.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Information

About this article

Publication history






Further reading