The potential for coupled organic and inorganic sulfur cycles across the terrestrial deep subsurface biosphere

Organosulfur compounds (OrgS) are fundamental components of life’s biomass, yet the cycling of these compounds in the terrestrial deep subsurface, one of Earth’s largest ecosystems, has gone relatively unexplored. Here, we show that all subsurface microbial genomes reconstructed from Soudan Underground Mine State Park have the capacity to cycle organic sulfur species. Our findings suggest that OrgS degradation may be an integral link between the organic and inorganic sulfur cycle via the production of sulfite and sulfide. Furthermore, despite isolation from surface ecosystems, most Soudan microorganisms retained genes for dimethylsulfoniopropionate and taurine biosynthesis. Metagenomic analyses of an additional 54 deep subsurface sites spanning diverse lithologies revealed the capacity for OrgS cycling to be widespread, occurring in 89% of assembled metagenomes. Our results indicate that consideration of OrgS cycling may be necessary to accurately constrain sulfur fluxes, discern the energetic limits of deep life, and determine the impact of deep subsurface biogeochemical sulfur cycling on greater Earth system processes.