Item

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
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.