The majority of microorganisms in gas hydrate-bearing subseafloor sediments ferment macromolecules

Background Gas hydrate-bearing subseafloor sediments harbor a large number of microorganisms. Sedimentary organic matter and upward methane fluids represent two important sources of carbon and energy for deep biosphere. However, which metabolism dominates the deep subseafloor of gas hydrate zone is poorly constrained. Here we studied the microbial communities in gas-hydrate rich sediments up to 49 meters below seafloor recovered by drilling in the South China Sea. We focused on distinct geochemical conditions, and performed metagenomic and metatranscriptomic analyses to characterize microbial diversity and their role in carbon mineralization. Results Comparative microbial community analysis revealed that samples above and in sulfate-methane interface (SMI) zones clearly distinguish from those below the SMI. Chloroflexota, are most abundant above the SMI, whereas Caldatribacteriota dominate below the SMI. Verrucomicrobiota, Bathyarchaeia and Hadarchaeota were similarly present in both types of sediment. The genomic inventory and transcriptional activity suggest roles in fermentation of macromolecule. By contrast, sulfate reducers and methanogens, organisms that catalyze the consumption or production of commonly observed chemical compounds in sediments are rare. Methanotrophs of the ANME-1 group thrived in or slightly below the current sulfate methane interface. Rare members from Heimdallarchaeia were identified to encode the potential for anaerobic oxidation of short-chain hydrocarbons. Conclusions These findings indicate that fermentation of macromolecules is the predominant energy source for microorganisms in deep subseafloor sediments that are experiencing upward methane fluxes.