Genome-encoded metabolic potential of the Nitrosocosmicus genus and related ammonia-oxidizing archaea

Abstract

Since the discovery of ammonia-oxidizing archaea (AOA), genomic and experimental evidence suggests that mixotrophic growth may complement chemolithotrophic ammonia oxidation for some AOA representatives. Although members of the Candidatus Nitrosocosmicus genus have been implicated in the use of alternate sources of energy and carbon, stronger genomic evidence is needed to support testing of hypotheses with robust experimental design. This study involved analysis of 58 genomes spanning all four known AOA groups (i.e., I.1a, I.1b, 1.1a-associated, thermophilic AOA; ThAOA). The analyses focused primarily on transporters and enzymes, linking the former to potential substrates from the transporter classification database (TCDB) and the latter to KEGG, Carbohydrate-Active enZYmes (CAZymes), and pathways from GapSeq. Correlated with genome size, the results demonstrate that genomes of the I.1b group, including those from the Ca. Nitrosocosmicus genus, showed the highest abundances of exclusive (only found within this group) and preferred (primarily associated with this group) proteins for alternative metabolism, followed by ThAOA, I.1a, and I.1a-associated. There was extensive functional heterogeneity among representative genomes, particularly for Ca. Nitrosocosmicus and Nitrososphaera genera. The group I.1b genomes encoded for the potential to use nitrogenous substrates such as urea, alanine, glycine, asparagine, and glutamine. Although Ca. Nitrosocosmicus genomes were more commonly associated with use of TCA cycle intermediates, such as citrate, malate, oxaloacetate, and succinate, this potential was likewise found in ThAOA and I.1a representatives. Several I.1b representative genomes encoded enzymes for metabolism of ureidoacrylates and carbamate, CAZymes associated with glycoside hydrolases, genes implying oxidation of sulfur and manganese, and polyamine metabolism. However, genes for synthesis and degradation of polyamines were common to many AOA genomes analyzed. Overall, the results suggest that I.1b-associated representatives encode for mixotrophic metabolism, and future research should verify associated substrate predictions experimentally. Given broad distributions of AOA within terrestrial and aquatic environments, these findings have implications for biogeochemical cycling of carbon and nitrogen on a global scale.