Sulfur disproportionating microbial communities in a dynamic, microoxic-sulfidic karst system

Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen-rich meteoric water, creating Proterozoic-like conditions and supporting a prolific sulfur-based lithoautotrophic ecosystem. To better understand the cycling of S0 in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide-oxidizing Beggiatoa mats. Sediment populations were dominated by uncultivated relatives of sulfur cycling lithoautotrophs related to Sulfurovum, Halothiobacillus, Thiofaba, Thiovirga, Thiobacillus, and Desulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated with Bacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae. Desulfocapsa populations accounted for 5-11% of sediment 16S rRNA amplicon sequences and were most closely related to D. thiozymogenes, which carries out autotrophic S0 disproportionation in pure culture. Gibbs energy calculations revealed that S0 disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat-sediment interface showed that Beggiatoa mats consume sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings strongly suggest that disproportionation is an important sink for S0 generated by microbial sulfide oxidation in this oxygen-limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur-rich environments.