Microbes in marine sediments represent a large portion of the biosphere, and resolving their ecology is crucial for understanding global ocean processes. Single-gene diversity surveys have revealed several uncultured lineages that are widespread in ocean sediments and whose ecological roles are unknown, and advancements in the computational analysis of increasingly large genomic data sets have made it possible to reconstruct individual genomes from complex microbial communities. Using these metagenomic approaches to characterize sediments is transforming our view of microbial communities on the ocean floor and the biodiversity of the planet. In recent years, marine sediments have been a prominent source of new lineages in the tree of life. The incorporation of these lineages into existing phylogenies has revealed that many belong to distinct phyla, including archaeal phyla that are advancing our understanding of the origins of cellular complexity and eukaryotes. Detailed comparisons of the metabolic potentials of these new lineages have made it clear that uncultured bacteria and archaea are capable of mediating key previously undescribed steps in carbon and nutrient cycling.

Gemmatimonadota bacteria are widely distributed in nature, but their metabolic potential and ecological roles in marine environments are poorly understood. Here, we obtained 495 metagenome-assembled genomes (MAGs), and associated viruses, from coastal to deep-sea sediments around the world. We used this expanded genomic catalog to compare the protein composition and update the phylogeny of these bacteria. The marine Gemmatimonadota are phylogenetically different from those previously reported from terrestrial environments. Functional analyses of these genomes revealed these marine genotypes are capable of degradation of complex organic carbon, denitrification, sulfate reduction, and oxidizing sulfide and sulfite. Interestingly, there is widespread genetic potential for secondary metabolite biosynthesis across Gemmatimonadota, which may represent an unexplored source of novel natural products. Furthermore, viruses associated with Gemmatimonadota have the potential to “hijack” and manipulate host metabolism, including the assembly of the lipopolysaccharide in their hosts. This expanded genomic diversity advances our understanding of these globally distributed bacteria across a variety of ecosystems and reveals genetic distinctions between those in terrestrial and marine communities.

Marine sediments comprise one of the largest environments on the planet, and their microbial inhabitants are significant players in global carbon and nutrient cycles. Recent studies using metagenomic techniques have shown the complexity of these communities and identified novel microorganisms from the ocean floor. Here, we obtained 77 metagenome-assembled genomes (MAGs) from the bacterial phylum Armatimonadota in the Guaymas Basin, Gulf of California, and the Bohai Sea, China. These MAGs comprise two previously undescribed classes within Armatimonadota, which we propose naming Hebobacteria and Zipacnadia. They are globally distributed in hypoxic and anoxic environments and are dominant members of deep-sea sediments (up to 1.95% of metagenomic raw reads). The classes described here also have unique metabolic capabilities, possessing pathways to reduce carbon dioxide to acetate via the Wood-Ljungdahl pathway (WLP) and generating energy through the oxidative branch of glycolysis using carbon dioxide as an electron sink, maintaining the redox balance using the WLP. Hebobacteria may also be autotrophic, not previously identified in Armatimonadota. Furthermore, these Armatimonadota may play a role in sulfur and nitrogen cycling, using the intermediate compounds hydroxylamine and sulfite. Description of these MAGs enhances our understanding of diversity and metabolic potential within anoxic habitats worldwide.