Brockarchaeota, a novel archaeal phylum with unique and versatile carbon cycling pathways

• Published in: Nature communications Vol. 12; no. 1; pp. 2404 - 12
• Main Authors: De Anda, Valerie, Chen, Lin-Xing, Dombrowski, Nina, Hua, Zheng-Shuang, Jiang, Hong-Chen, Banfield, Jillian F., Li, Wen-Jun, Baker, Brett J.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23.04.2021; Nature Publishing Group; Nature Portfolio
• Subjects: 45; 49; 49/23; 631/158/855; 631/181/2480; 631/326/26/2142; 631/326/26/2526; Archaea - classification; Archaea - genetics; Archaea - metabolism; archaeal genomics; Arsenic; BASIC BIOLOGICAL SCIENCES; Carbon; Carbon - metabolism; Carbon cycle; Carbon Cycle - genetics; China; Classification; Deep sea; Deep sea environments; ENVIRONMENTAL SCIENCES; Fermenters; Genome, Archaeal - genetics; Genomes; Genotypes; Geography; Geologic Sediments - microbiology; Glycine; Hot springs; Hot Springs - microbiology; Humanities and Social Sciences; Hydrothermal vents; Hydrothermal Vents - microbiology; Mercury; Mercury (metal); Metabolism; Metagenome - genetics; metagenomics; Methane - metabolism; microbial ecology; Microorganisms; multidisciplinary; Phosphorylation; Phylogeny; Plants; Polysaccharides; RNA, Ribosomal, 16S - genetics; Saccharides; Science; Science (multidisciplinary); Sediments; Species Specificity; Substrates; taxonomy; Tetrahydrofolic acid; Trimethylamine; Vents; China
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-021-22736-6

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. Geothermal environments are hotspots for carbon cycling. Here, De Anda et al. reconstruct archaeal genomes from terrestrial and deep-sea geothermal sediments, and propose the classification of these microbes as a new phylum, ‘Brockarchaeota’, with unique metabolic capabilities including non-methanogenic anaerobic methylotrophy.