Genomic traits and biogeographic pattern reflect adaptation of the Atlantic Ocean microbiome to Nitrogen availability and acquisition

Nitrogen (N) limits phytoplankton primary production in large areas of the oceans. Hence its availability and forms of occurrence are crucial for evolutionary adaptation of microbes to N acquisition and growth at varying N regimes. To examine how genomic traits reflect these adaptations we analyzed the genomic GC content and N atoms per amino acid side residue side chain and occurrence of gene clusters encoding N acquisition pathways in the sunlit Atlantic Ocean microbiome between 62 °S and 47 °N. The mean genomic GC content of the entire prokaryotic communities ranged from 36 to 44% with highest percentages in the northern- and southernmost regions and lowest percentages in tropical regions. Several prominent groups, such as Rhodobacterales, SAR86, SAR92, followed the general trend with reduced GC-percentages in N-depleted and enhanced GC-percentages in N-rich regions, reflecting adaptations to different N availabilities. Pelagibacterales, Prochlorococcus and Flavobacterales exhibited consistently low genomic GC-percentages, whereas Sphingobacterales showed consistently high genomic GC-percentages. The genomes of the SAR116 cluster, Verrucomicrobia and Synechococcus varied in their GC-percentages across the transect, but not related to N-availability and thus suggesting that other factors control their N acquisition.

Genes encoding amino acid, dipeptide, oligopeptide and ammonium transport, cyanate lyase, formamidase, urease, nitrate and nitrite reductase and N-fixation exhibited distinct biogeographic patterns and were distributed differently among bacterial phylogenetic lineages, reflecting their potential traits to acquire N in the available forms under the prevailing biogeographic conditions. Whereas for some of these N-compounds concentrations and uptake rate measurements are available for others, like di- and oligopeptides, cyanate and formamide, they need to be developed for a comprehensive understanding of their role in ocean biogeochemistry.