From temperate to polar waters: Transition to non-cyanobacterial diazotrophy upon entering the Atlantic gateway of the Arctic Ocean

Abstract

Nitrogen fixation, the microbial reduction of dinitrogen to ammonia, is increasingly recognized to occur in the Arctic Ocean. However, knowledge about the composition, biogeography, abundance, and ecology of nitrogen-fixing organisms (diazotrophs) is poor. This ultimately hinders prediction of ecosystem productivity fueled by nitrogen fixation in this rapidly changing and predominantly nitrogen-limited ocean. We assessed the composition and abundance of total and active diazotrophs in sub-surface water (8 m; amplicon sequencing and quantification of the marker gene nifH) over [~]3,400 km from the mouth of the brackish Baltic Sea to the sea ice edge in the Arctic Ocean. Upon entering nutrient-rich waters in the Atlantic gateway to the Arctic, we discovered an abrupt transition from autotrophic to heterotrophic diazotrophic activity. Our findings suggest that diazotrophy is functionally distinct in the Arctic Ocean compared to adjacent temperate-boreal waters - a difference likely driven by inorganic nutrients, salinity, and temperature. We identify three key non-cyanobacterial diazotroph groups in the Arctic Ocean with Arctic-specific (Rhodocyclales and Oceanospirillales) or more widespread (unknown Gammaproteobacterium) distribution patterns and report their nifH gene transcription levels (up to 103 nifH transcripts L-1). In contrast, actively transcribing diazotrophs in the warmer and more nutrient-poor Norwegian Sea with coastal-influenced water were dominated by sublineages of Candidatus Atelocyanobacterium thalassa (UCYN-A1, UCYN-A2, UCYN-A4; up to 104 nifH transcripts L-1). With ongoing atlantification of the Arctic pushing oceanic provinces and biogeographical ranges poleward, we predict a future displacement of the transition from autotrophic to heterotrophic diazotrophic activity with likely significant changes in nitrogen fixation.