Microbial consumption of zero-valence sulfur in marine benthic habitats

Zero-valence sulfur (S0) is a central intermediate in the marine sulfur cycle and occurs in significant amounts at sediment surfaces, hydrothermal vents and in oxygen minimum zones. While diverse isolated strains use S0 for energy conservation, those microorganisms consuming S0 in the environment are largely unknown. Via the 16S rRNA approach we identified microbial key players in S0-turnover in three contrasting, marine benthic habitats: i) tidal sediments, ii) deep-sea volcanogenic S0 and iii) deep-sea S0-precipitating microbial mats. Regardless of the habitat the epsilonproteobacterial Sulfurimonas/Sulfurovum-group accounted for a dominant fraction of the microbial community on native or introduced S0. Sulfate production by S0-grown biofilms and S0-enrichments strongly suggested that this group autotrophically oxidized S0. Deltaproteobacterial Desulfobulbaceae and Desulfuromonadales were also frequently detected, indicating S0-disporpotionation and S0-reduction under oxygen-depleted conditions. Our study highlights the previously overlooked, but central role of Sulfurimonas/Sulfurovum-related Epsilonproteobacteria for S0-conversion in non-hydrothermal habitats at the sea floor. Particularly in coastal sediments, the ability to access S0 equips them with a competitive advantage over other, more abundant sulfur oxidizers. Such niche partitioning among sulfur oxidizers is novel and could explain their environmental coexistence.