The evolution and spread of sulfur cycling enzymes reflect the redox state of the early Earth

The biogeochemical sulfur cycle plays a central role in fueling microbial metabolisms, regulating the Earth's redox state, and affecting climate. However, geochemical reconstructions of the ancient sulfur cycle are confounded by ambiguous isotopic signals. We use phylogenetic reconciliation to ascertain the timing of ancient sulfur cycling gene events across the tree of life. Our results suggest that metabolisms using sulfide oxidation emerged in the Archean, but those involving thiosulfate emerged only after the Great Oxidation Event. Our data reveal that observed geochemical signatures resulted not from the expansion of a single type of organism but were instead associated with genomic innovation across the biosphere. Moreover, our results provide the first indication of organic sulfur cycling from the Mid-Proterozoic onwards, with implications for climate regulation and atmospheric biosignatures. Overall, our results provide insights into how the biological sulfur cycle evolved in tandem with the redox state of the early Earth.

Automated summary

The biogeochemical sulfur cycle plays a central role in microbial metabolisms, Earth's redox state regulation, and climate effects. Geochemical reconstructions of the ancient sulfur cycle are complicated due to ambiguous isotopic signals. By using phylogenetic reconciliation, we determined the timing of ancient sulfur cycling gene events across the tree of life. Our findings suggest the early emergence of sulfide oxidation metabolisms in the Archean, while thiosulfate-based metabolisms emerged after the Great Oxidation Event. These results highlight the contribution of genomic innovation to the observed geochemical signatures and reveal the existence of organic sulfur cycling since the Mid-Proterozoic, with implications for climate regulation and atmospheric biosignatures. Overall, our study provides insights into the co-evolution of biological sulfur cycle and early Earth's redox state.