Microorganisms have driven Earth’s sulfur cycle since the emergence of life1–6, yet the sulfur-cycling capacities of microorganisms and their integration with other element cycles remain incompletely understood. One such uncharacterized metabolism is the coupling of sulfide oxidation with iron(iii) oxide reduction, a ubiquitous environmental process hitherto considered to be strictly abiotic7,8. Here we present a comprehensive genomic analysis of sulfur metabolism across prokaryotes, and reveal bacteria that are capable of oxidizing sulfide using extracellular solid phase iron(iii). Based on a phylogenetic framework of over hundred genes involved in dissimilatory transformation of sulfur compounds, we recorded sulfur-cycling capacity in most bacterial and archaeal phyla. Metabolic reconstructions predicted co-occurrence of sulfur compound oxidation and iron(iii) oxide respiration in diverse members of 37 prokaryotic phyla. Physiological and transcriptomic evidence demonstrated that a cultivated representative, Desulfurivibrio alkaliphilus, grows autotrophically by oxidizing dissolved sulfide or iron monosulfide (FeS) to sulfate with ferrihydrite as an extracellular iron(iii) electron acceptor. The biological process outpaced the abiotic process at environmentally relevant sulfide concentrations. These findings expand the known diversity of sulfur-cycling microorganisms and unveil a biological mechanism that links sulfur and iron cycling in anoxic environments, thus highlighting the fundamental role of microorganisms in global element cycles.
