Evans, Paul N.

Marine sediments are vast, underexplored habitats and represent one of the largest carbon deposits on our planet. Microbial communities drive nutrient cycling in these sediments, but the full extent of their taxonomic and metabolic diversity remains to be explored. Here, we analysed shallow coastal and deep subseafloor sediment cores from 0.01 to nearly 600 metres below the seafloor, in the Western Pacific Region. Applying metagenomics, we identified several taxonomic clusters across all samples, which mainly aligned with depth and sediment type. Inferring functional patterns provided insights into possible ecological roles of the main microbial taxa. These included Chloroflexota, the most abundant phylum across all samples, whereby the classes Dehalococcoida and Anaerolineae dominated deep-subsurface and most shallow coastal sediments, respectively. Thermoproteota and Asgardarchaeota were the most abundant phyla among Archaea, contributing to high relative abundances of Archaea reaching over 50% in some samples. We recovered high-quality metagenome-assembled genomes for all main prokaryotic lineages and proposed names for three phyla, i.e. Tangaroaeota phyl. nov. (former RBG-13-66-14), Ryujiniota phyl. nov. (former UBA6262) and Spongiamicota phyl. nov. (former UBA8248). Metabolic capabilities across all samples ranged from aerobic respiration and photosynthesis in the shallowest sediment layers to heterotrophic carbon utilization, sulphate reduction and methanogenesis in deeper anoxic sediments. We also identified taxa with the potential to be involved in nitrogen and sulphur cycling and heterotrophic carbon utilization. In summary, this study contributes to our understanding of the taxonomic and functional diversity in benthic prokaryotic communities across marine sediments in the Western Pacific Region.

AbstractSeveral recent studies have shown the presence of genes for the key enzyme associated with archaeal methane/alkane metabolism, methyl-coenzyme M reductase (Mcr), in metagenome-assembled genomes (MAGs) divergent to existing archaeal lineages. Here, we study the mcr-containing archaeal MAGs from several hot springs, which reveal further expansion in the diversity of archaeal organisms performing methane/alkane metabolism. Significantly, an MAG basal to organisms from the phylum Thaumarchaeota that contains mcr genes, but not those for ammonia oxidation or aerobic metabolism, is identified. Together, our phylogenetic analyses and ancestral state reconstructions suggest a mostly vertical evolution of mcrABG genes among methanogens and methanotrophs, along with frequent horizontal gene transfer of mcr genes between alkanotrophs. Analysis of all mcr-containing archaeal MAGs/genomes suggests a hydrothermal origin for these microorganisms based on optimal growth temperature predictions. These results also suggest methane/alkane oxidation or methanogenesis at high temperature likely existed in a common archaeal ancestor.

AbstractChallenges in cultivating microorganisms have limited the phylogenetic diversity of currently available microbial genomes. This is being addressed by advances in sequencing throughput and computational techniques that allow for the cultivation-independent recovery of genomes from metagenomes. Here, we report the reconstruction of 7,903 bacterial and archaeal genomes from >1,500 public metagenomes. All genomes are estimated to be ≥50% complete and nearly half are ≥90% complete with ≤5% contamination. These genomes increase the phylogenetic diversity of bacterial and archaeal genome trees by >30% and provide the first representatives of 17 bacterial and three archaeal candidate phyla. We also recovered 245 genomes from the Patescibacteria superphylum (also known as the Candidate Phyla Radiation) and find that the relative diversity of this group varies substantially with different protein marker sets. The scale and quality of this data set demonstrate that recovering genomes from metagenomes provides an expedient path forward to exploring microbial dark matter.

AbstractMethanogenesis is the primary biogenic source of methane in the atmosphere and a key contributor to climate change. The long-standing dogma that methanogenesis originated within the Euryarchaeota was recently challenged by the discovery of putative methane-metabolizing genes in members of the Bathyarchaeota, suggesting that methanogenesis may be more phylogenetically widespread than currently appreciated. Here, we present the discovery of divergent methyl-coenzyme M reductase genes in population genomes recovered from anoxic environments with high methane flux that belong to a new archaeal phylum, the Verstraetearchaeota. These archaea encode the genes required for methylotrophic methanogenesis, and may conserve energy using a mechanism similar to that proposed for the obligate H2-dependent methylotrophic Methanomassiliicoccales and recently described Candidatus ‘Methanofastidiosa’. Our findings indicate that we are only beginning to understand methanogen diversity and support an ancient origin for methane metabolism in the Archaea, which is changing our understanding of the global carbon cycle.