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

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-based1–5. 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 −46h 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 133S values between −1.65 and +1.43h and δ34S values ranging from −12 to +6h 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. Evidence of cellular organization would represent one of the strongest lines of evidence for a Palaeoarchean biosphere, but this has been beset with controversy7,8. At present, microbial mats9–11 together with sulphur isotope analysis1–5 provide the best insights into Palaeoarcheanmicrobial metabolisms and ecosystems, with evidence reported for phototrophs9–11 plus hydrogen-based10 and sulphur-based1–5 metabolisms. However, these reports lack evidence for accompanying cellular morphology. Here, we provide such evidence in the form of well-preserved cells closely associated with pyrite in the basal sandstone member of the ∼3,400Myr-old Strelley Pool Formation (SPF),Western Australia. The SPF crops out across eleven greenstone belts within the East Pilbara Terrane, spanning a ∼75Myr hiatus in volcanism between the 3,520–3,427Myr-old Warrawoona Group and the 3,350–3,315Myr-old Kelly Group12. Our microfossils come from the East Strelley greenstone belt (Supplementary Fig. S1), where the SPF lies above an unconformity on top of eroded ∼3,515Myrold volcanics13. Here, the SPF records a marine transgression across one of Earth’s earliest preserved shorelines, with the basal sandstone deposited in a shallow-water beach or estuarine setting14, and the overlying carbonates deposited in a marine carbonate platform setting11,15. Early silica cements in the sandstones include isopachous phreatic cements (Supplementary Fig. S2),