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

Journal name:
Nature Geoscience
Volume:
4,
Pages:
698–702
Year published:
DOI:
doi:10.1038/ngeo1238
Received
Accepted
Published online

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.

At a glance

Figures

  1. Examples of spheroidal/ellipsoidal microfossils from the SPF (samples SP9D2, SPE1, SPV3a-c).
    Figure 1: Examples of spheroidal/ellipsoidal microfossils from the SPF (samples SP9D2, SPE1, SPV3a–c).

    a,b,e, Clusters of cells, some showing cell wall rupturing (arrows in a,b), folding or invagination (arrow in e). c,d,h, Chains of cells with cellular divisions (arrows). f,ij, Cells attached to detrital quartz grains, exhibiting cell wall rupturing and putative escape of cell contents (arrow in f), preferred alignment of cells parallel to the surface of the quartz grain (arrows in i), and constriction or folding between two compartments (arrow in j). g, Large cellular compartment with folded walls (arrows).

  2. Examples of hollow, tubular, sheath-like microfossils from the SPF (samples SPV3a-c).
    Figure 2: Examples of hollow, tubular, sheath-like microfossils from the SPF (samples SPV3a-c).

    a, Tubes (arrows) extending away from a detrital quartz grain (dashed surface). b, Three partially degraded aligned tubes (1–3). c, Tube with a split wall (arrow), co-occurring with clusters of spheroidal microfossils. d, Montaged transverse cross-sections through two tubes (boxed) occurring with pyrite (P), permitting clear differentiation from spheroidal cells, or potentially non-biological artefacts. e, Dense patch of tubes with two examples (arrows) in an approximate longitudinal section. f, Biofilm coating detrital quartz grain with a long tubular microfossil (boxed) and pyrite (P arrow).

  3. Microfossil walls and quartz grain boundaries (sample SPV3b).
    Figure 3: Microfossil walls and quartz grain boundaries (sample SPV3b).

    a,b, Bright-field- and energy-filtered-TEM images of a partial cell wall (from Fig. 1f). Carbon is confined to the curved cell wall. Multiple micro-quartz grains infill the cell interior, confirmed by selected area electron diffraction patterns (1–4) showing a changing orientation of crystallographic axes across (dashed) grain boundaries. The speckled wall ultrastructure plus discrete quartz grains (arrowed) suggest partial permineralization of the microfossil wall by silica. c, Dark-field scanning-TEM image of a directly comparable microfossil wall from the 1,878Myr-old Gunflint Formation. Intensities inverted so that carbon is white (modified from ref. 22).

  4. Spatial relationships between microfossils and pyrite (SP9D2a-b, SPV3b).
    Figure 4: Spatial relationships between microfossils and pyrite (SP9D2a–b, SPV3b).

    a, Partial microfossil walls (black arrows) intermixed with pyrite coating quartz grains. Pyrite (right image, white) occurs as 1–10μm grains exterior to the microfossils and as nano-grains within microfossil walls (white arrows). b, TEM images of a partial microfossil wall showing pyrite occurring as sub-micrometre grains within and adjacent to the wall. c, NanoSIMS maps of nitrogen (26CN) and sulphur (32S) showing a putative spheroidal microfossil (arrow) associated with micrometre-sized pyrite. d, Spheroidal microfossil associated with pyrite (P), exhibiting a partially preserved ‘double wall’ and putative expulsion of cellular contents (arrow).

References

  1. Shen, Y., Buick, R. & Canfield, D. E. Isotopic evidence for microbial sulphate reduction in the early Archean era. Nature 410, 7781 (2001).
  2. Philippot, P. et al. Early Archaean microorganisms preferred elemental sulfur, not sulfate. Science 317, 15341537 (2007).
  3. Ueno, Y., Ono, S., Rumble, D. & Maruyama, S. 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, 56755691 (2008).
  4. Shen, Y., Farquhar, J., Masterson, A., Kaufman, A. J. & Buick, R. Evaluating the role of microbial sulfate reduction in the early Archean using quadruple isotope systematics. Earth Planet. Sci. Lett. 279, 383391 (2009).
  5. Wacey, D., McLoughlin, N., Whitehouse, M. J. & Kilburn, M. R. Two coexisting sulfur metabolisms in a ca. 3400Ma sandstone. Geology 38, 11151118 (2010).
  6. Javaux, E. J., Marshall, C. P. & Bekker, A. Organic-walled microfossils in 3.2 billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934938 (2010).
  7. Schopf, J. W. Microfossils of the Early Archean Apex Chert: New evidence for the antiquity of life. Science 260, 640646 (1993).
  8. Brasier, M. D. et al. Questioning the evidence for Earth’s oldest fossils. Nature 416, 7681 (2002).
  9. Tice, M. M. & Lowe, D. R. Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431, 549552 (2004).
  10. Tice, M. M. & Lowe, D. R. Hydrogen-based carbon fixation in the earliest known photosynthetic organisms. Geology 34, 3740 (2006).
  11. 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, 714718 (2006).
  12. Hickman, A. H. Regional review of the 3426–3350Ma Strelley Pool Formation, Pilbara Craton, Western Australia. Geol. Surv. W.A. Rec 2008/15, 27 (Geological Survey of Western Australia, 2008).
  13. Buick, R. et al. Record of emergent continental crust ~3.5 billion years ago in the Pilbara Craton of Australia. Nature 375, 574577 (1995).
  14. Wacey, D. et al. The ~3.4 billion-year-old Strelley Pool sandstone: A new window into early life on Earth. Int. J. Astrobiol. 5, 333342 (2006).
  15. Van Kranendonk, M. J., Webb, G. E. & Kamber, B. S. Geological and trace element evidence for a marine sedimentary environment of deposition and biogenicity of 3.45Ga stromatolitic carbonates in the Pilbara Craton, and support for a reducing Archean ocean. Geobiology 1, 91108 (2003).
  16. Tucker, M. E. Sedimentary Petrology 3rd edn 263 (Blackwell Science, 2001).
  17. Sugitani, K. et al. Biogenicity of morphologically diverse carbonaceous microstructures from the ca. 3400Ma Strelley Pool Formation, in the Pilbara Craton. West. Aust. Astrobiol. 10, 899920 (2010).
  18. Tice, M. M., Bostick, B. C. & Lowe, D. R. 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, 3740 (2004).
  19. Wyckoff, R. W. G. Crystal Structures 2nd edn, Vol. 1 (Wiley, 1963).
  20. Van Kranendonk, M. J. 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. Simonson, B. M. Early silica cementation and subsequent diagenesis in arenites from four early Proterozoic iron formations of North America. J. Sedim. Res. 57, 494511 (1987).
  22. Moreau, J. W. & Sharp, T. G. A transmission electron microscopy study of silica and kerogen biosignatures in ~1.9Ga Gunflint microfossils. Astrobiology 4, 196210 (2004).
  23. Schopf, J. W. in The Precambrian Earth: Tempos and Events (eds Eriksson, P. G., Altermann, W., Nelson, D. R., Mueller, W. U. & Catuneanu, O.) 516539 (Elsevier, 2004).
  24. Schopf, J. W. Fossil evidence of Archaean life. Phil. Trans. R. Soc. B 361, 869885 (2006).
  25. Brasier, M. D., McLoughlin, N., Green, O. & Wacey, D. A fresh look at the fossil evidence for early Archaean cellular life. Phil. Trans. R. Soc. B 361, 887902 (2006).
  26. Noffke, N. Microbial Mats in Sandy Deposits from the Archean Era to Today 194 (Springer, 2010).
  27. Schidlowski, M. A 3,800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333, 313318 (1988).
  28. Wacey, D., Saunders, M., Brasier, M. D. & Kilburn, M. R. Earliest microbially mediated pyrite oxidation in ~3.4 billion-year-old sediments. Earth Planet. Sci. Lett. 301, 393402 (2011).
  29. Kusakabe, M., Komoda, Y., Takano, B. & Abiko, T. 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, 287307 (2000).
  30. Moreau, J. W., Webb, R. I. & Banfield, J. F. Ultrastructure, aggregation-state, and crystal growth of biogenic nanocrystalline sphalerite and wurtzite. Am. Mineral. 89, 950960 (2004).

Download references

Author information

Affiliations

  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

Contributions

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 financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (1.60 MB)

    Supplementary Information

Additional data