Anaerobic Degradation of Non-Methane Alkanes by Candidatus Methanoliparia in Hydrocarbon Seeps of the Gulf of Mexico

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. IMPORTANCE Oil-rich sediments from the Gulf of Mexico were found to contain diverse alkane- degrading groups of archaea. The symbiotic, consortium-forming Candidatus Argoarchaeum and Candidatus Syntrophoarchaeum are likely responsible for the degradation of ethane and short-chain alkanes, with the help of sulfate- reducing bacteria. Ca. Methanoliparia occurs as single cells associated with oil droplets. These archaea encode two phylogenetically different methylcoenzyme M reductases that may allow this organism to thrive as a methanogen on a substrate of long-chain alkanes. Based on a library survey, we show that Ca. Methanoliparia is frequently detected in oil reservoirs and may be a key agent in the transformation of long-chain alkanes to methane. Our findings provide evidence for the important and diverse roles of archaea in alkane-rich marine habitats and support the notion of a significant functional versatility of the methyl coenzyme M reductase.