ALBERT

Description: Cold seeps and hydrothermal vents deliver large amounts of methane and other gaseous alkanes into marine surface sediments. Consortia of archaea and partner bacteria thrive on the oxidation of these alkanes and its coupling to sulfate reduction. The inherently slow growth of the involved organisms and the lack of pure cultures have impeded the understanding of the molecular mechanisms of archaeal alkane degradation. Here, using hydrothermal sediments of the Guaymas Basin (Gulf of California) and ethane as the substrate, we cultured microbial consortia of a novel anaerobic ethane oxidizer, “Candidatus Ethanoperedens thermophilum” (GoM-Arc1 clade), and its partner bacterium “Candidatus Desulfofervidus auxilii,” previously known from methane-oxidizing consortia. The sulfate reduction activity of the culture doubled within one week, indicating a much faster growth than in any other alkane-oxidizing archaea described before. The dominance of a single archaeal phylotype in this culture allowed retrieval of a closed genome of “Ca. Ethanoperedens,” a sister genus of the recently reported ethane oxidizer “Candidatus Argoarchaeum.” The metagenome-assembled genome of “Ca. Ethanoperedens” encoded a complete methanogenesis pathway including a methyl-coenzyme M reductase (MCR) that is highly divergent from those of methanogens and methanotrophs. Combined substrate and metabolite analysis showed ethane as the sole growth substrate and production of ethyl-coenzyme M as the activation product. Stable isotope probing demonstrated that the enzymatic mechanism of ethane oxidation in “Ca. Ethanoperedens” is fully reversible; thus, its enzymatic machinery has potential for the biotechnological development of microbial ethane production from carbon dioxide.

Description: Crude oil and gases in the seabed provide an important energy source for subsurface microorganisms. We investigated the role of archaea in the anaerobic degradation of non-methane alkanes in deep-sea oil seeps from the Gulf of Mexico. We identified microscopically the ethane and short-chain alkane oxidizers “Candidatus Argoarchaeum” and “Candidatus Syntrophoarchaeum” forming consortia with bacteria. Moreover, we found that the sediments contain large numbers of cells from the archaeal clade “Candidatus Methanoliparia,” which was previously proposed to perform methanogenic alkane degradation. “Ca. Methanoliparia” occurred abundantly as single cells attached to oil droplets in sediments without apparent bacterial or archaeal partners. Metagenome-assembled genomes of “Ca. Methanoliparia” encode a complete methanogenesis pathway including a canonical methyl-coenzyme M reductase (MCR) but also a highly divergent MCR related to those of alkane-degrading archaea and pathways for the oxidation of long-chain alkyl units. Its metabolic genomic potential and its global detection in hydrocarbon reservoirs suggest that “Ca. Methanoliparia” is an important methanogenic alkane degrader in subsurface environments, producing methane by alkane disproportionation as a single organism.