Potential for microbial anaerobic hydrocarbon degradation in naturally petroleum-associated deep-sea sediments

The lack of cultured isolates and microbial genomes from the deep seabed means that very little is known about the ecology of this vast habitat. Here, we investigated energy and carbon acquisition strategies of microbial communities from three deep seabed petroleum seeps (3 km water depth) in the Eastern Gulf of Mexico. Shotgun metagenomic analysis revealed that each sediment harbored diverse communities of chemoheterotrophs and chemolithotrophs. We recovered 82 metagenome-assembled genomes affiliated with 21 different archaeal and bacterial phyla. Multiple genomes encoded enzymes for acetogenic fermentation of aliphatic and aromatic compounds, specifically those of candidate phyla Aerophobetes, Aminicenantes, TA06 and Bathyarchaeota. Microbial interactions in these communities are predicted to be driven by acetate and molecular hydrogen, as indicated by a high abundance of fermentation, acetogenesis, and hydrogen utilization pathways. These findings are supported by sediment geochemistry, metabolomics and thermodynamic modelling of hydrocarbon degradation. Overall, we infer that deep-sea sediments experiencing thermogenic hydrocarbon inputs harbor phylogenetically and functionally diverse communities potentially sustained through anaerobic hydrocarbon, acetate and hydrogen metabolism.