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

Abstract

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 methyl-coenzyme 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.

“ Candidatus Ethanoperedens,” a Thermophilic Genus of Archaea Mediating the Anaerobic Oxidation of Ethane

“…Ethanoperedens" is phylogenetically most closely related to the recently described divergent-type MCR of "Ca. Argoarchaeum" with an amino acid identity of 69% but also with all other mcrA sequences of GoM-Arc1 archaea (5,12,16,18). These MCRs form a distinct cluster in comparison to other divergent MCRs and to the canonical MCRs of methanogens and methanotrophs (Fig.…”

“…Argoarchaeum" have been found in hydrocarbon-rich marine environments like cold-seep and hot-vent environments, including asphalt seeps in the Gulf of Mexico and the Guaymas Basin hydrothermal vents in the Gulf of California (31)(32)(33). In some environments like oil seeps of the Gulf of Mexico and gas-rich barite chimneys of Loki's Castle, 16S rRNA gene surveys have shown that up to 30% of archaeal gene sequences belonged to the GoM-Arc1 clade (12). To estimate absolute abundances and potential partnerships of GoM-Arc1 in the environment, we performed CARD-FISH on samples from different seep and vent sites across the globe (Fig.…”

Methyl/alkyl‐coenzyme M reductase‐based anaerobic alkane oxidation in archaea

“…Syntrophoarchaeum and potential other long-chain alkane degraders, the formed acyl-CoA is first subjected to betaoxidation, then the produced acetyl-CoA is oxidized via the Wood-Ljungdahl pathway (Fig. 3A, Laso -Pérez et al, 2016-Pérez et al, , 2019Wang et al, 2019a). The beta-oxidation pathway is widespread in all domains of life, and it can also be used in the generation of fatty acid (Dibrova et al, 2014).…”

Marine Sediments Harbor Diverse Archaea and Bacteria With Potentials for Anaerobic Hydrocarbon Degradation via Fumarate Addition

“…Bacteria and archaea capable of anaerobic hydrocarbon degradation are widely distributed and are not limited to hydrocarbon-rich environments. It is not surprising that hydrocarbon-degrading microorganisms are most prevalent in sediments featuring natural seepage of oil and gas, due to high concentrations of hydrocarbons at these sites [23,48,49]. However, in subsurface sediments that do not feature seepage, relatively high abundances of hydrocarbon degraders are also observed ( Fig.…”