Genomic profiling of Nitrospira species reveals ecological success of comammox Nitrospira

BACKGROUND: The discovery of microorganisms capable of complete ammonia oxidation to nitrate (comammox) has prompted a paradigm shift in our understanding of nitrification, an essential process in N cycling, hitherto considered to require both ammonia oxidizing and nitrite oxidizing microorganisms. This intriguing metabolism is unique to the genus Nitrospira, a diverse taxon previously known to only contain canonical nitrite oxidizers. Comammox Nitrospira have been detected in diverse environments; however, a global view of the distribution, abundance, and diversity of Nitrospira species is still incomplete. RESULTS: In this study, we retrieved 55 metagenome-assembled Nitrospira genomes (MAGs) from newly obtained and publicly available metagenomes. Combined with publicly available MAGs, this constitutes the largest Nitrospira genome database to date with 205 MAGs, representing 132 putative species, most without cultivated representatives. Mapping of metagenomic sequencing reads from various environments against this database enabled an analysis of the distribution and habitat preferences of Nitrospira species. Comammox Nitrospira's ecological success is evident as they outnumber and present higher species-level richness than canonical Nitrospira in all environments examined, except for marine and wastewaters samples. The type of environment governs Nitrospira species distribution, without large-scale biogeographical signal. We found that closely related Nitrospira species tend to occupy the same habitats, and that this phylogenetic signal in habitat preference is stronger for canonical Nitrospira species. Comammox Nitrospira eco-evolutionary history is more complex, with subclades achieving rapid niche divergence via horizontal transfer of genes, including the gene encoding hydroxylamine oxidoreductase, a key enzyme in nitrification. CONCLUSIONS: Our study expands the genomic inventory of the Nitrospira genus, exposes the ecological success of complete ammonia oxidizers within a wide range of habitats, identifies the habitat preferences of (sub)lineages of canonical and comammox Nitrospira species, and proposes that horizontal transfer of genes involved in nitrification is linked to niche separation within a sublineage of comammox Nitrospira. Video Abstract.