Methane production from hydrocarbons by consortia dominated by ANME archaea

Abstract

Understanding microbial production and consumption of methane, a potent greenhouse gas in the atmosphere, is critical for bridging knowledge gaps in global carbon cycling. In anoxic environments, methane is known to be produced through hydrogenotrophic, acetoclastic or methylotrophic mechanisms. Methane production from hydrocarbons may also be important, especially in hydrocarbon-rich environments, like the Gulf of California, but the mechanism of this hydrocarbonoclastic methanogenesis remains unclear. The activity of consortia of anaerobic methane oxidizing (ANME) archaea and bacteria limits the release of methane to the atmosphere by consuming methane in anoxic environments globally. Here we used isotopic-labeling to track the conversion of hydrocarbons (hexadecane and naphthalene) to methane in enrichments from hydrothermally impacted, hydrocarbon-rich sediments from the Gulf of California. Methane was produced directly from hexadecane and naphthalene, in both the presence and absence of sulfate. We reconstructed metagenomic assembled-genomes (MAGs) from these experiments which revealed a mixture of bacteria dominated by Desulfobacteriota and Bacteroidota, and archaea dominated by Aeinigmarchaeota, Thermoplasmatota, and ANME group 2c. The ANME-2c were the only MAGs that encoded methyl coenzyme M reductases (McrA) and complete Wood-Ljungdahl pathways (WLP). This suggests that ANME-2c archaea may be involved in the production of methane along the seafloor, and that our understanding of the roles of these globally important microbes is not yet fully appreciated.