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Surveys of 16S rRNA gene sequences derived from marine sediments have indicated that a widely distributed group of Gammaproteobacteria , named “JTB255-Marine Benthic Group” (now the candidate order Woeseiales ), accounts for 1–22% of the retrieved sequences. Despite their ubiquity in seafloor communities, little is known about their distribution and specific ecological niches in the deep sea, which constitutes the largest biome globally. Here, we characterized the phylogeny, environmental distribution patterns, abundance, and metabolic potential of Woeseiales bacteria with a focus on representatives from the deep sea. From a phylogenetic analysis of publicly available 16S rRNA gene sequences (≥1400 bp, n  = 994), we identified lineages of Woeseiales with greater prevalence in the deep sea than in coastal environments, a pattern corroborated by the distribution of 16S oligotypes recovered from 28 globally distributed sediment samples. Cell counts revealed that Woeseiales bacteria accounted for 5 ± 2% of all microbial cells in deep-sea surface sediments at 23 globally distributed sites. Comparative analyses of a genome, metagenome bins, and single-cell genomes suggested that members of the corresponding clades are likely to grow on proteinaceous matter, potentially derived from detrital cell membranes, cell walls, and other organic remnants in marine sediments.

Methane seeps are widespread seafloor ecosystems shaped by the emission of gas from seabed reservoirs. The microorganisms inhabiting methane seeps transform the chemical energy in methane to products that sustain rich benthic communities around the gas leaks. Despite the biogeochemical relevance of microbial methane removal at seeps, the global diversity and dispersion of seep microbiota remain unknown. Here we determined the microbial diversity and community structure of 23 globally distributed methane seeps and compared these to the microbial communities of 54 other seafloor ecosystems, including sulfate–methane transition zones, hydrothermal vents, coastal sediments, and deep-sea surface and subsurface sediments. We found that methane seep communities show moderate levels of microbial richness compared with other seafloor ecosystems and harbor distinct bacterial and archaeal taxa with cosmopolitan distribution and key biogeochemical functions. The high relative sequence abundance of ANME (anaerobic methanotrophic archaea), as well as aerobic Methylococcales , sulfate-reducing Desulfobacterales , and sulfide-oxidizing Thiotrichales , matches the most favorable microbial metabolisms at methane seeps in terms of substrate supply and distinguishes the seep microbiome from other seafloor microbiomes. The key functional taxa varied in relative sequence abundance between different seeps due to the environmental factors, sediment depth and seafloor temperature. The degree of endemism of the methane seep microbiome suggests a high local diversification in these heterogeneous but long-lived ecosystems. Our results indicate that the seep microbiome is structured according to metacommunity processes and that few cosmopolitan microbial taxa mediate the bulk of methane oxidation, with global relevance to methane emission in the ocean. Significance Methane seeps are natural gas leaks at the seafloor that emit methane to the hydrosphere. The emission rates are controlled by methane-oxidizing microorganisms, which shape the ecosystem by supplying energy sources to other microorganisms and animal symbioses. We provide evidence that methane seeps are island-like habitats, harboring distinct microbial communities that share few organisms with other seafloor ecosystems. The seep communities comprise bacteria and archaea that occur worldwide but are locally selected by the environment. These microorganisms show high relative sequence abundances, suggesting high population densities and global relevance for the control of methane emission from the seafloor. At individual seeps, the cosmopolitan microorganisms are associated with a substantial diversity of rare relatives, turning seeps into hotspots of microbial biodiversity.

The anaerobic formation and oxidation of methane involve unique enzymatic mechanisms and cofactors, all of which are believed to be specific for C 1 -compounds. Here we show that an anaerobic thermophilic enrichment culture composed of dense consortia of archaea and bacteria apparently uses partly similar pathways to oxidize the C 4 hydrocarbon butane. The archaea, proposed genus ‘ Candidatus Syntrophoarchaeum’, show the characteristic autofluorescence of methanogens, and contain highly expressed genes encoding enzymes similar to methyl-coenzyme M reductase. We detect butyl-coenzyme M, indicating archaeal butane activation analogous to the first step in anaerobic methane oxidation. In addition, Ca . Syntrophoarchaeum expresses the genes encoding β-oxidation enzymes, carbon monoxide dehydrogenase and reversible C 1 methanogenesis enzymes. This allows for the complete oxidation of butane. Reducing equivalents are seemingly channelled to HotSeep-1, a thermophilic sulfate-reducing partner bacterium known from the anaerobic oxidation of methane. Genes encoding 16S rRNA and methyl-coenzyme M reductase similar to those identifying Ca . Syntrophoarchaeum were repeatedly retrieved from marine subsurface sediments, suggesting that the presented activation mechanism is naturally widespread in the anaerobic oxidation of short-chain hydrocarbons. Anaerobic archaea enriched in thermophilic microbial consortia completely degrade butane by modifying mechanisms which were hitherto thought to be specific to methane metabolism. Environmental oxidation of non-methane hydrocarbons Research on the anaerobic oxidation of natural gas has largely been focused on methane as the most abundant constituent. It is less clear how short-chain alkanes—including ethane, propane, n -butane and iso -butane, which together make up about 20% of natural gas—are anaerobically metabolized. Sulfate-reducing bacteria are the only organisms known to date to anaerobically oxidize short-chain hydrocarbons. Gunter Wegener and colleagues identify an anaerobic thermophilic enrichment culture composed of dense consortia of archaea and bacteria that uses a pathway similar to anaerobic methane oxidation, which was previously thought to be specific for C 1 -compounds, to oxidize butane. Archaea activate butane, and reducing equivalents are channelled to sulfate-reducing partner bacteria. Similar consortia are detected in marine subsurface sediments, suggesting that this pathway may be widespread in nature.

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. 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 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 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.

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. 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.

The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. AOM is performed by microbial consortia of archaea (ANME) associated with partners related to sulfate-reducing bacteria. In vitro enrichments of AOM were so far only successful at temperatures ⩽25 °C; however, energy gain for growth by AOM with sulfate is in principle also possible at higher temperatures. Sequences of 16S rRNA genes and core lipids characteristic for ANME as well as hints of in situ AOM activity were indeed reported for geothermally heated marine environments, yet no direct evidence for thermophilic growth of marine ANME consortia was obtained to date. To study possible thermophilic AOM, we investigated hydrothermally influenced sediment from the Guaymas Basin. In vitro incubations showed activity of sulfate-dependent methane oxidation between 5 and 70 °C with an apparent optimum between 45 and 60 °C. AOM was absent at temperatures ⩾75 °C. Long-term enrichment of AOM was fastest at 50 °C, yielding a 13-fold increase of methane-dependent sulfate reduction within 250 days, equivalent to an apparent doubling time of 68 days. The enrichments were dominated by novel ANME-1 consortia, mostly associated with bacterial partners of the deltaproteobacterial HotSeep-1 cluster, a deeply branching phylogenetic group previously found in a butane-amended 60 °C-enrichment culture of Guaymas sediments. The closest relatives ( Desulfurella spp.; Hippea maritima ) are moderately thermophilic sulfur reducers. Results indicate that AOM and ANME archaea could be of biogeochemical relevance not only in cold to moderate but also in hot marine habitats.

The methane-rich, hydrothermally heated sediments of the Guaymas Basin are inhabited by thermophilic microorganisms, including anaerobic methane-oxidizing archaea (mainly ANME-1) and sulfate-reducing bacteria (e.g., HotSeep-1 cluster). We studied the microbial carbon flow in ANME-1/ HotSeep-1 enrichments in stable-isotope–probing experiments with and without methane. The relative incorporation of ¹³C from either dissolved inorganic carbon or methane into lipids revealed that methane-oxidizing archaea assimilated primarily inorganic carbon. This assimilation is strongly accelerated in the presence of methane. Experiments with simultaneous amendments of both ¹³C-labeled dissolved inorganic carbon and deuterated water provided further insights into production rates of individual lipids derived from members of the methane-oxidizing community as well as their carbon sources used for lipid biosynthesis. In the presence of methane, all prominent lipids carried a dual isotopic signal indicative of their origin from primarily autotrophic microbes. In the absence of methane, archaeal lipid production ceased and bacterial lipid production dropped by 90%; the lipids produced by the residual fraction of the metabolically active bacterial community predominantly carried a heterotrophic signal. Collectively our results strongly suggest that the studied ANME-1 archaea oxidize methane but assimilate inorganic carbon and should thus be classified as methane-oxidizing chemoorganoautotrophs.

Notes how the methane-emitting cold seeps of Hikurangi margin (New Zealand) are among the few deep-sea chemosynthetic ecosystems of the Southern Hemisphere known to date. Compares the biogeochemistry and microbial communities of a variety of Hikurangi cold seep ecosystems. Includes highly reduced seep habitats dominated by bacterial mats, partially oxidized habitats populated by heterotrophic ampharetid polychaetes and deeply oxidized habitats dominated by chemosynthetic frenulate tubeworms. Source: National Library of New Zealand Te Puna Matauranga o Aotearoa, licensed by the Department of Internal Affairs for re-use under the Creative Commons Attribution 3.0 New Zealand Licence.

Coastal sands are biocatalytic filters for dissolved and particulate organic matter of marine and terrestrial origin, thus, acting as centers of organic matter transformation. At high temporal resolution, we accessed the variability of benthic bacterial communities over two annual cycles at Helgoland (North Sea), and compared it with seasonality of communities in Isfjorden (Svalbard, 78°N) sediments, where primary production does not occur during winter. Benthic community structure remained stable in both, temperate and polar sediments on the level of cell counts and 16S rRNA-based taxonomy. Actinobacteriota of uncultured Actinomarinales and Microtrichales were a major group, with 8 ± 1% of total reads (Helgoland) and 31 ± 6% (Svalbard). Their high activity (frequency of dividing cells 28%) and in situ cell numbers of >10% of total microbes in Svalbard sediments, suggest Actinomarinales and Microtrichales as key heterotrophs for carbon mineralization. Even though Helgoland and Svalbard sampling sites showed no phytodetritus-driven changes of the benthic bacterial community structure, they harbored significantly different communities (p < 0.0001, r = 0.963). The temporal stability of benthic bacterial communities is in stark contrast to the dynamic succession typical of coastal waters, suggesting that pelagic and benthic bacterial communities respond to phytoplankton productivity very differently.

Background 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 two microbial communities is limited due to the complexity of benthic microbiomes. Results Here, we used a long-reads (LRs) metagenomic approach to examine benthic microbiomes and compared them to the microbiomes in the overlaying water column and on particles, sampled at the same site and time off the island Heligoland in the North Sea. Although the diversity is vast in marine sediments, we recovered high quality metagenome assembled genomes (MAGs). Based on taxonomy and metabolic annotation of predicted proteins, benthic microbiomes are distinctly different from pelagic microbiomes. When comparing the 270 MAGs from free living and particle attached microbes from the water column to 115 MAGs from sediments only 2 MAGs affiliated to Acidimicrobiia and Desulfocapsaceae were shared at species level. Although, we recovered MAGs with the same taxonomic annotation in pelagic and benthic microbiomes, their metabolic potentials were different. A prominent example was the family Woeseiaceae that was among the most abundant taxa in the sediments. In benthic Woeseiaceae MAGs, we found polysaccharide utilization loci (PULs), predicted to target laminarin, alginate, and α-glucan. In contrast, pelagic Woeseiaceae MAGs were only recovered in the particle attached but not in the free-living fraction, and lacked PULs. They encoded a significantly more sulfatases and peptidases genes. Additionally, while genes involved in iron acquisition, gene regulation, and iron storage were widespread in Woeseiaceae MAGs, genes linked to dissimilatory iron reduction were mostly restricted to benthic Woeseiaceae , suggesting niche-specific adaptations to sediment redox conditions. Both, benthic and pelagic particle-attached Woeseiaceae MAGs encoded pilus TadA genes, which are essential for adhesion, colonization, and biofilm formation. Conclusions LR sequencing is currently the most valuable tool for analyzing highly diverse benthic microbiomes. The small overlap of MAGs from water column and sediments indicated a limited bentho-pelagic coupling. The data suggest that Woeseiaceae have habitat-specific metabolic specialization: while benthic Woeseiaceae possess the metabolic capabilities to utilize fresh organic compounds like laminarin derived from algae blooms, and to perform dissimilatory nitrate, nitrite and iron reduction for gain energy, particle attached Woeseiaceae from the water column may be specialized in degrading protein-rich and sulfated organic matter likely reflecting adaptation to the different types of organic matter and redox conditions in sediments vs. the water column.