Global evolutionary pattern and distinct metabolic strategies of sulfur-cycling microorganisms across ecosystems

Microorganisms drive the global sulfur cycle, but the complexity of sulfur redox transformations complicates understanding of their evolution, metabolism, and ecology. We developed DiSuCy, a manually curated, phylogeny-aware knowledgebase of 116 dissimilatory sulfur metabolism genes to identify sulfur-cycling microorganisms in (meta)genomes/transcriptomes. Key sulfur metabolism genes showed varying evolutionary conservation and intermediate horizontal transfer rates, enabling taxonomically scaled predictions of sulfur metabolisms. Co-occurrence of sulfur metabolisms with other biochemical pathways was shaped by redox thermodynamics, defining metabolic niches and ecosystem specificity of sulfur-cycling microorganisms. We predicted previously unrecognized sulfur-cycling members across underexplored bacterial phyla, thiotrophs respiring nitrate/arsenate or utilizing light, and ocean and human gut microbiomes. Some non-canonical sulfur taxa abundantly transcribed pathways for methanethiol oxidation in the global ocean or reduced sulfur compound oxidation in the gut. These findings expand the toolkit for studying sulfur-cycling microorganisms and provide new insights into their evolutionary dynamics and ecology.