Unique phylogenies and metabolic adaptations of novel lineage III and comammox Nitrospira species from deep-sea sediments

Abstract The genus Nitrospira, which includes canonical nitrite-oxidizing bacteria (NOB) and species capable of complete ammonia oxidation (comammox), plays an important role in the global biogeochemical nitrogen cycle. Typically, lineage IV Nitrospira predominate in marine environments, and other lineages are thought to be less abundant and remain poorly characterized in oceanic systems. Here, we recovered five novel metagenome-assembled genomes (MAGs) affiliated with Nitrospira lineage II–IV from deep-sea sediments. Notably, two of these MAGs represent members of lineage III and comammox Nitrospira, respectively, suggesting the presence of previously uncharacterized lineages in the deep sea. Phylogenetic and gene locus analyses indicated that deep-sea lineage III and comammox Nitrospira form distinct evolutionary clades that diverge from their terrestrial and coastal relatives, and we therefore designate these two marine-derived groups as “lineage III clade B” and “comammox clade A4”, respectively. Comparative read recruitment analyses revealed that these lineages exhibit potential pan-oceanic distribution in deep-sea sediments and waters, albeit at very low abundances. Furthermore, the identification of genes encoding amtB-type ammonium transporters (amtB), the ABC-type glycerol-3-phosphate transport system (ugpABCE), a multi-subunit Na+/H+ antiporter (mnh), and betaine transporters (BetT, opuABC) suggests that these newly discovered Nitrospira species possess adaptive capabilities to thrive in oligotrophic and saline marine environments. These findings provide novel insights into the occurrence, metabolic features, and adaptation strategies of lineage III and comammox Nitrospira, expand our understanding of Nitrospira diversity in the deep sea, and offer valuable perspectives on the evolutionary history of various Nitrospira lineages.