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Abstract

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 Glade), 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.
IMPORTANCE In the seabed, gaseous alkanes are oxidized by syntrophic
microbial consortia that thereby reduce fluxes of these compounds into
the water column. Because of the immense quantities of seabed alkane
fluxes, these consortia are key catalysts of the global carbon cycle.
Due to their obligate syntrophic lifestyle, the physiology of
alkane-degrading archaea remains poorly understood. We have now
cultivated a thermophilic, relatively fast-growing ethane oxidizer in
partnership with a sulfate-reducing bacterium known to aid in methane
oxidation and have retrieved the first complete genome of a short-chain
alkane-degrading archaeon. This will greatly enhance the understanding
of nonmethane alkane activation by noncanonical methyl-coenzyme M
reductase enzymes and provide insights into additional metabolic steps
and the mechanisms underlying syntrophic partnerships. Ultimately, this
knowledge could lead to the biotechnological development of alkanogenic
microorganisms to support the carbon neutrality of industrial processes.