Distribution and survival strategies of endemic and cosmopolitan diazotrophs in the Arctic Ocean

Dinitrogen (N-2) fixation is the major source of reactive nitrogen in the ocean and has been considered to occur specifically in low-latitude oligotrophic oceans. Recent studies have shown that N-2 fixation also occurs in the polar regions and thus is a global process, although the physiological and ecological characteristics of polar diazotrophs are not yet known. Here, we successfully reconstructed diazotroph genomes, including that of cyanobacterium UCYN-A (Candidatus 'Atelocyanobacterium thalassa'), from metagenome data corresponding to 111 samples isolated from the Arctic Ocean. These diazotrophs were highly abundant in the Arctic Ocean (max., 1.28% of the total microbial community), suggesting that they have important roles in the Arctic ecosystem and biogeochemical cycles. Further, we show that diazotrophs within genera Arcobacter, Psychromonas, and Oceanobacter are prevalent in the <0.2 mu m fraction in the Arctic Ocean, indicating that current methods cannot capture their N-2 fixation. Diazotrophs in the Arctic Ocean were either Arctic-endemic or cosmopolitan species from their global distribution patterns. Arctic-endemic diazotrophs, including Arctic UCYN-A, were similar to low-latitude-endemic and cosmopolitan diazotrophs in genome-wide function, however, they had unique gene sets (e.g., diverse aromatics degradation genes), suggesting adaptations to Arctic-specific conditions. Cosmopolitan diazotrophs were generally non-cyanobacteria and commonly had the gene that encodes the cold-inducible RNA chaperone, which presumably makes their survival possible even in deep, cold waters of global ocean and polar surface waters. This study shows global distribution pattern of diazotrophs with their genomes and provides clues to answering the question of how diazotrophs can inhabit polar waters.

Automated summary

Dinitrogen (N-2) fixation is considered to occur only in low-latitude oceans, but recent studies have found that it also occurs in polar regions, indicating it is a global process. This study successfully reconstructed diazotroph genomes from samples in the Arctic Ocean and found that they are highly abundant and play important roles in the Arctic ecosystem and biogeochemical cycles. Diazotrophs in the Arctic Ocean are either Arctic-endemic or cosmopolitan species and have unique gene sets that enable them to adapt to Arctic-specific conditions.