Anammox bacteria inhabiting oxygen deficient zones (ODZs) are a critical functional group mediating fixed nitrogen loss in the global ocean. However, the diversity, broad metabolisms, origin, and adaptive mechanisms of anammox bacteria in this dynamic environment remain unknown. Here we address these questions by recovering high-quality genomes of anammox bacteria from global ODZs and comparing them to their sediment counterparts. We recovered two novel metagenome-assembled genomes of anammox bacteria affiliated with the Scalindua genus (Candidatus Scalindua praevalens and Candidatus Scalindua variabilis), which represent most, if not all, of the anammox bacteria in the global ODZs. They are ubiquitously present in all three major ODZs. Beyond the core anammox metabolism, both organisms contain cyanase and the more dominant one encodes a urease, indicating most ODZ anammox bacteria can utilize cyanate and urea in addition to ammonium. Molecular clock analysis suggests that the evolutionary radiation of these bacteria into ODZs occurred no earlier than 310 million years ago, about one billion years after the emergence of the earliest modern-type ODZs. Different strains of the ODZ Scalindua species are also found in benthic sediments, and the first ODZ Scalindua likely derived from the benthos. Compared to benthic strains, ODZ Scalindua uniquely encode genes for urea utilization but have lost genes related to growth arrest, flagellum synthesis, and chemotaxis, presumably for adaptation to thrive in the global ODZ waters. Our findings expand the known metabolism and constrain the evolutionary history of the bacteria controlling the global nitrogen budget.

anammox, oxygen deficient zones, nitrogen biogeochemistry, genome evolution