Anaerobic methanotrophic communities thrive in deep submarine permafrost

Thawing submarine permafrost is a source of methane to the subsurface biosphere. Methane oxidation in submarine permafrost sediments has been proposed, but the responsible microorganisms remain uncharacterized. We analyzed archaeal communities and identified distinct anaerobic methanotrophic (ANME-2a/b, ANME-2d) assemblages in frozen and completely thawed submarine permafrost sediments. Besides archaea potentially involved in AOM we found a large diversity of archaea mainly belonging to Bathyarchaeota , Thaumarchaeota , and Euryarchaeota . Methane concentrations and δ 13 C-methane signatures distinguish horizons of potential anaerobic oxidation of methane (AOM) coupled either to sulfate reduction in a sulfate-methane transition zone (SMTZ) or to the reduction of other electron acceptors, such as iron, manganese or nitrate. Analysis of functional marker genes ( mcrA ) and fluorescence in situ hybridization (FISH) corroborate AOM communities in submarine permafrost sediments potentially active at low temperatures. Extrapolating potential AOM rates, when scaled to the total area of expected submarine permafrost thaw, reveals that methane could be consumed at rates between 8 and 120 Tg C per year, which is comparable to other AOM habitats such as seeps, continental SMTZ and wetlands. We thus propose that AOM is active where submarine permafrost thaws and needs to be accounted for in global methane budgets.