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

Abstract

AbstractThe biogeochemical sulfur cycle plays a central role in fueling microbial metabolisms, regulating the redox state of the Earth, and impacting climate through remineralization of organic carbon. However, traditional reconstructions of the ancient sulfur cycle based on geochemistry are confounded by ambiguous isotopic signals, low sulfate concentrations in the Archean ocean, and the isotopic impacts of photolysis acting on volcanogenic SO2gas. Here, we use a phylogenomics approach to ascertain the timing of gene speciation, duplication, loss, and horizontal gene transfer events for sulfur cycling genes across the tree of life. Our results suggest that metabolisms using sulfate reduction and sulfide oxidation emerged in the Archean, but metabolic pathways involving thiosulfate and thesoxpathway proliferated across the tree of life only after the Great Oxidation Event, suggesting enhanced recycling of sulfur with increasing oxygen levels in the Paleoproterozoic ocean. We also identified a late-Proterozoic spread of these metabolisms, possibly linked to Neoproterozoic or Paleozoic ocean oxygenation. Our data go beyond geochemical records by revealing that the manifestations of geochemical signatures resulted not from the expansion of a single type of organism, but were instead associated with the expansion of genomic innovation across the biosphere. Moreover, our results provide the first indication of organic sulfur cycling from the mid-Proterozoic onwards. The formation of DMS may have had implications for climate regulation and atmospheric biosignatures. Overall, our results provide new insights into how the biological sulfur cycle evolved in tandem with the redox state of the early Earth.TeaserPhylogenomics analyses reveal that the evolution of microbial sulfur metabolisms coevolved with the redox state of the surface environment of the early Earth.