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

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Nature Geoscience
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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


  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).


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  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


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.

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