The archaeal symbiotic Nanobdellales have been isolated with their hosts from a shallow hot marine vent off Iceland and from terrestrial hot springs in Yellowstone National Park and Japan. They have highly reduced genomes and rely on their archaeal hosts for most of their metabolic needs. Here, to provide further insights into the ecology and evolution of this order, we greatly expand their phylogenomic distribution using metagenome-assembled genomes from deep-sea hydrothermal vents in the Atlantic, Pacific and Indian Oceans, and the Gulf of California. We show that at least 11 novel genus-level lineages occur at deep-sea vents. We conservatively propose two new genera with their nomenclatural types, Nanoprofundum liuii Rb-1Ts gen. nov. sp. nov. and Nanojejuna irisiana Rb-38Ts gen. nov. sp. nov. We also describe a second species of Nanoarchaeum, N. abyssimaris 17S-22Ts sp. nov. Our genomic and metabolic characterization of the high-quality metagenome-assembled genomes confirm their highly reduced metabolic capabilities and likely symbiotic lifestyle. With the exception of Nanoarchaeum, all deep-sea genera resemble their terrestrial relatives in that they have genes that encode for archaella and RNAase P protein subunits, and have several genes involved in glycolysis and gluconeogenesis. Using an inferred lateral gene transfer analysis, our data suggest that deep-sea Nanobdellales may potentially associate with a greater taxonomic breadth of hosts than previously reported, spanning members of the Sulfolobales (Ignicoccaceae), the Archaeoglobales and Methanococcales.
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