Knittel, K. | bioRxiv Science

bioRxiv2024

Deep long-read metagenomic sequencing reveals niche differentiation in carbon cycling potential between benthic and planktonic microbial populations

Coastal marine sediments function as large-scale natural biocatalytic filters, remineralizing and transforming organic matter. Benthic microbiomes exhibit remarkable temporal stability, contrasting with the dynamic, substrate-driven successions of bacterioplankton. Nonetheless, understanding their role in carbon cycling and interactions between these microbial groups is limited due to the complexity of benthic microbiomes. Here, we used a seasonally resolved, deep short- and long-read metagenomic approach to examine distinctive genomic features of microbiomes recovered from sediment, the overlaying water column, and particle-attached bacteria and archaea in the North Sea. We recovered 115 benthic metagenome-assembled genomes (MAGs) that belonged to Woeseiales, Rhizobiales, Planctomycetia, Gemmatimonadota, and Desulfobacterota species. While Proteobacteria and Actinobacteriota were characteristic phyla of sediments, Acidimicrobiia and Desulfocapsaceae species were shared between sediments and particle-attached fractions of the water column, indicative of significant bentho-pelagic coupling. Predominant members of the family Woeseiaceae carried polysaccharide utilization loci (PULs) predicted to target laminarin, alginate, and -glucan in sediments. In contrast, water column species lacked PULs and encoded a significantly higher fraction of sulfatases and peptidases, indicating a role in the degradation of protein-rich and sulfated organic matter. Our findings disentangle family-level adaptations and niche differentiation between globally significant benthic and water column populations involved in marine organic matter degradation and carbon storage.

microbiology↗

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↗