Endemic dark ocean microbiomes drive carbon cycling in the Southern Ocean

The Southern Ocean hosts a high degree of endemic plants and animals, yet the genetic diversity, function and evolutionary relationships of microbial communities remains unexplored, particularly in the aphotic “dark ocean,” where microbes play critical roles in local and global food webs. Here, we performed a metagenomic analysis of 44 aphotic seawater samples collected from multiple depths across the Southern Ocean to characterize the functional gene repertoire of these microbial communities. Of the 11,896,546 species-level unigenes¹ identified, ~ 87% appear specific to the Southern Ocean and are distinct from other major ocean datasets. We reconstructed 502 bacterial and 108 archaeal metagenome-assembled genomes (MAGs), revealing widespread capacities for inorganic carbon fixation via the Calvin cycle, the hydroxypropionate-hydroxybutyrate cycle, and the 3-hydroxypropionate bi-cycle. Metapangenomic analyses indicated that several genes involved in the oxidation of reduced nutrients including ammonia, nitrite, and thiosulfate, are shared across the aphotic water column through horizontal gene transfer. MAGs belonging to Acidimicrobia, Gammaproteobacteria, and SAR324 were abundant throughout the dark Southern Ocean and showed potential for both chemolithoautotrophy and carbohydrate degradation, suggesting mixotrophy as a key metabolic strategy. Together, these findings reveal the unique functional and genomic diversity of deep Southern Ocean microbiomes and provide insights into their roles in carbon cycling within one of Earth’s most important marine carbon sinks.