Sulfur disproportionation occurs globally across anoxic habitats and has multiple mechanisms of independent evolutionary origin

Microbial sulfur disproportionation is a unique and enigmatic pathway of energy metabolism in bacteria where a single intermediate sulfur species, e.g. elemental sulfur, is simultaneously oxidized and reduced while generating ATP. We do not have a complete picture of the molecular mechanisms underlying microbial sulfur disproportionation and several pathways are likely involved depending on the taxon. This impairs our ability to investigate the evolutionary history, antiquity, taxonomic distribution, and ecological significance of this metabolism. Here we provide a comprehensive overview of all previously proposed candidate genes, translation of some of which is upregulated under sulfur disproportionation conditions, as well as other sulfur-utilizing dissimilatory metabolic pathways, across the diversity of all genomically characterized sulfur-disproportionating bacteria from a wide range of environments, and phylogenetically reconstruct their evolutionary history. We conclude that the MOLY cluster of likely extracellular molybdopterin oxidoreductases and the YTD cluster of mostly uncharacterized proteins are currently the best candidates for sulfur disproportionation markers in Desulfobacterota and Nitrospirota, and confirm previous observations that other taxa likely use different mechanisms. We also show that sulfur disproportionation pathways utilize enzymes from other processes of sulfur metabolism. The most parsimonious scenario for evolutionary origins of MOLY and YTD clusters is their presence already in the last common ancestor of Desulfobacterota, Nitrospirota, and Acidobacteriota, which lived in the Paleoarchean. Our analyses substantially narrow down the field of viable candidate genes and provide directions for future research.