Hassenrück, Christiane

Abstract Sandy sediments of the coastal ocean are generally not considered a habitat for highly active sulfate-reducing microorganisms (SRM) 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 SRM may contribute to higher levels of sulfate reduction than previously assumed in the extensive areas of permeable sediments of coastal and shelf seas.

Abstract Background Rare species, especially of the marine sedimentary biosphere, have long been overlooked owing to the complexity of sediment microbial communities, their sporadic temporal and patchy spatial abundance, and challenges in cultivating environmental microorganisms. In this study, we combined enrichments, targeted metagenomic sequencing, and extensive data mining to uncover uncultivated members of the archaeal rare biosphere in marine sediments. Results In protein-amended enrichments, we detected the ecologically and metabolically uncharacterized class Candidatus Penumbrarchaeia within the phylum Thermoplasmatota. By screening more than 8000 metagenomic runs and 11,479 published genome assemblies, we expanded the phylogeny of Ca. Penumbrarchaeia by 3 novel orders. All six identified families of this class show low abundance in environmental samples characteristic of rare biosphere members. Members of the class Ca. Penumbrarchaeia were predicted to be involved in organic matter degradation in anoxic, carbon-rich habitats. All Ca. Penumbrarchaeia families contain high numbers of taxon-specific orthologous genes, highlighting their environmental adaptations and habitat specificity. Besides, members of this group exhibit the highest proportion of unknown genes within the entire phylum Thermoplasmatota, suggesting a high degree of functional novelty in this class. Conclusions In this study, we emphasize the necessity of targeted, data-integrative approaches to deepen our understanding of the rare biosphere and uncover the functions and metabolic potential hidden within these understudied taxa.