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Geothermal environments, such as hot springs and hydrothermal vents, are hotspots for carbon cycling and contain many poorly described microbial taxa. Here, we reconstructed 15 archaeal metagenome-assembled genomes (MAGs) from terrestrial hot spring sediments in China and deep-sea hydrothermal vent sediments in Guaymas Basin, Gulf of California. Phylogenetic analyses of these MAGs indicate that they form a distinct group within the TACK superphylum, and thus we propose their classification as a new phylum, 'Brockarchaeota', named after Thomas Brock for his seminal research in hot springs. Based on the MAG sequence information, we infer that some Brockarchaeota are uniquely capable of mediating non-methanogenic anaerobic methylotrophy, via the tetrahydrofolate methyl branch of the Wood-Ljungdahl pathway and reductive glycine pathway. The hydrothermal vent genotypes appear to be obligate fermenters of plant-derived polysaccharides that rely mostly on substrate-level phosphorylation, as they seem to lack most respiratory complexes. In contrast, hot spring lineages have alternate pathways to increase their ATP yield, including anaerobic methylotrophy of methanol and trimethylamine, and potentially use geothermally derived mercury, arsenic, or hydrogen. Their broad distribution and their apparent anaerobic metabolic versatility indicate that Brockarchaeota may occupy previously overlooked roles in anaerobic carbon cycling.

Metagenomics of marine sediments has uncovered a broad diversity of new uncultured taxa and provided insights into their metabolic capabilities. Here, we detected microbial lineages from a sediment core near the Jiulong methane reef of the northern South China Sea (at 1,100-m depth). Assembly and binning of the metagenomes resulted in 11 genomes (>85% complete) that represented nine distinct phyla, including candidate phyla TA06 and LCP-89, Lokiarchaeota , Heimdallarchaeota , and a newly described globally distributed phylum (B38). The genome of LCP-89 has pathways for nitrate, selenate, and sulfate reduction, suggesting that they may be involved in mediating these important processes. B38 are able to participate in the cycling of hydrogen and selenocompounds. Many of these uncultured microbes may also be capable of autotrophic CO 2 fixation, as exemplified by identification of the Wood-Ljungdahl (W-L) pathway. Genes encoding carbohydrate degradation, W-L pathway, Rnf-dependent energy conservation, and Ni/Fe hydrogenases were detected in the transcriptomes of these novel members. Characterization of these new lineages provides insight to the undescribed branches in the tree of life. IMPORTANCE Sedimentary microorganisms in the South China Sea (SCS) remain largely unknown due to the complexity of sediment communities impacted by continent rifting and extension. Distinct geochemical environments may breed special microbial communities including microbes that are still enigmatic. Functional inference of their metabolisms and transcriptional activity provides insight in the ecological roles and substrate-based interactivity of these uncultured Archaea and Bacteria These microorganisms play different roles in utilizing inorganic carbon and scavenging diverse organic compounds involved in the deep-sea carbon cycle. The genomes recovered here contributed undescribed species to the tree of life and laid the foundation for future study on these novel phyla persisting in marginal sediments of the SCS., (Copyright © 2019 American Society for Microbiology.)