The evolution and spread of sulfur-cycling enzymes across the tree of life through deep time

The 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. Understanding the evolutionary history of the biological sulfur cycle can offer important insights into the redox state of our planet over time as well as the evolution of microbial life on Earth. However, most geochemical studies of the ancient sulfur cycle have been constrained by weak isotopic signals, low sulfate concentrations in the Archean ocean, and the isotopic impacts of photolysis acting on volcanogenic SO2 gas. Here, we use a phylogenomics approach to ascertain the timing of gene 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 early in life’s evolution, but metabolic pathways involving thiosulfate and the sox pathway proliferated across the tree of life only after the Great Oxidation Event. Moreover, our results provide the first indication of organic sulfur cycling in the Archean. Overall, our results provide new insights into how the biological sulfur cycle evolved in tandem with the redox state of the early Earth and illustrate the power of combining geochemical and bioinformatics approaches to understand the evolution of Earth over time.