A Bacterial Pathway for Homotaurine Catabolism via Sulfopropanoate

Small aminoorganosulfonates are reservoirs of carbon, nitrogen, and sulfur in marine and host-associated ecosystems. Homotaurine, a C3-aminoorganosulfonate produced by marine algae and present in algal-derived foods, is comparatively well documented, but its complete microbial catabolism has remained unresolved. Here we identify a complete bacterial pathway for homotaurine catabolism in Caballeronia jiangsuensis strain McCoy, isolated by metabolic enrichment from soil by growth on homotaurine. Growth, proteomic, metabolomic, biochemical, structural, and heterologous-expression analyses show that homotaurine is imported and oxidatively deaminated to sulfopropanoate, then converted to sulfolactate through E-sulfoacrylate by SpuABCD and SpuIJ, enzymes related to succinate dehydrogenase and fumarase. Sulfolactate is cleaved by redundant SuyAB sulfolyases to release pyruvate and sulfite, which is oxidized and excreted as sulfate, completing biomineralization. Crystal structures of the HtaA homotaurine-binding protein and SuyAB2 sulfolyase reveal ligand recognition and provide a structural framework for sulfolactate cleavage. Hidden Markov model searches and Tara Oceans and human gut metagenomes show that the core sulfopropanoate-to-sulfolactate module is widespread in marine Proteobacteria, especially Roseobacter-lineage bacteria, and occurs more narrowly in human gut-associated sulfur-metabolizing taxa such as Bilophila wadsworthia. This pathway connects algal, dietary, and xenobiotic C3-aminoorganosulfonates to microbial carbon, nitrogen, and sulfur cycling, and identifies sulfopropanoate turnover as a conserved module in organosulfonate metabolism.