Teske, A. | Search bioRxiv

bioRxiv2020

The Guaymas Basin Subseafloor Sedimentary Archaeome Reflects Complex Environmental Histories

We explore archaeal distribution and environmental niche differentiation in sedimentary subseafloor habitats of Guaymas Basin and the adjacent Sonora Margin, located in the Gulf of California, Mexico. Specifically, we survey diverse subseafloor habitats on the Guaymas Basin flanking regions that are extending from the spreading center, termed here "off-axis" sites. Sampling locations include (i) control sediments without hydrothermal or seep influence, (ii) Sonora Margin sediments underlying oxygen minimum zone water, (iii) compacted, highly reduced sediments from a pressure ridge with numerous seeps at the base of the Sonora Margin, and (iv) sediments impacted by hydrothermal circulation at the off-axis Ringvent site. Generally, archaeal 16S rRNA gene datasets are largely comprised of Bathyarchaeal lineages, members of the Hadesarchaea, MBG-D, TMEG, and ANME-1 groups. The most frequently observed 25 OTUs belong to members of these lineages, and correspond to approx. 40 to 80% of the sequence dataset in each sediment sample. Differential distribution patterns of these archaeal groups in downcore sediments uniquely characterize each major sedimentary environment. Variations in archaeal community composition reflect locally specific environmental challenges throughout the greater Guaymas Basin area. Background sediments are divided into surface and subsurface niches, reflecting increased selection of the archaeal community downcore. In sum, the environmental setting and history of a particular site, not isolated biogeochemical properties out of context, control the subseafloor archaeal communities in Guaymas Basin and Sonora Margin sediments.

ecology↗

bioRxiv2020

Candidatus Ethanoperedens, a thermophilic genus of archaea mediating the anaerobic oxidation of ethane

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 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 retrieving 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 for 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 sole growth substrate and production of ethyl-coenzyme M as activation product. Stable isotope probing showed that the enzymatic mechanisms 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. IMPORTANCEIn 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 non-methane alkane activation by non-canonical 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. EtymologyEthanoperedens. ethano, (new Latin): pertaining to ethane; peredens (Latin): consuming, devouring; thermophilum. (Greek): heat-loving. The name implies an organism capable of ethane oxidation at elevated temperatures. LocalityEnriched from hydrothermally heated, hydrocarbon-rich marine sediment of the Guaymas Basin at 2000 m water depth, Gulf of California, Mexico. DiagnosisAnaerobic, ethane-oxidizing archaeon, mostly coccoid, about 0.7 m in diameter, forms large irregular cluster in large dual-species consortia with the sulfate-reducing partner bacterium Candidatus Desulfofervidus auxilii.

microbiology↗