A novel Thermodesulfovibrionia lineage largely supports sulfate reduction in sandy sediments of the southern Baltic Sea

Abstract Sandy sediments of the coastal ocean are generally not considered a habitat for highly active sulfate-reducing microorganisms due to fluctuations in oxygen concentrations and carbon availability. This study investigated the taxonomic composition and gene expression patterns of sulfate-reducing communities in both sandy, organic-poor sediments and muddy, organic-rich sediments in the mesohaline southern Baltic Sea. Our results revealed that a novel order-level lineage within the class Thermodesulfovibrionia (phylum Nitrospirota), named Arenidesulfomonadales, contributed significantly to sulfate reduction in the sandy sediments and supported sulfate reduction rates similar to those in the organic-rich muddy sediments. In the sands, Thermodesulfovibrionia effectively competed with Desulfobacterales, which strongly dominated the sulfate-reducing communities in the organic-rich sediments. Metatranscriptomic data revealed that Desulfobacterales functioned as typical secondary fermenters in both sediment types and expressed nearly complete sets of genes for the catabolism of fermentation products such as lactate, propionate, and butyrate. In contrast, the gene expression profile of Thermodesulfovibrionia suggests that hydrogenotrophic sulfate reduction, coupled with carbon fixation via the Wood-Ljungdahl pathway and a reduced capacity to oxidize organic compounds, was a competitive metabolic strategy enabling sulfate reduction to proceed independently of fermentation-derived carbon. Overall, our results suggest that overlooked lineages of sulfate-reducing microorganisms may contribute to higher levels of sulfate reduction than previously assumed in the extensive areas of permeable sediments of coastal and shelf seas.