Synechococcus nitrogen gene loss in iron-limited ocean regions

Abstract

Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptation to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose nitrate and nitrite assimilation gene loss in Synechococcus represents an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export. SignificanceThe cyanobacterium Synechococcus is a major contributor to ocean primary production and biogeochemistry. Here, we used quantitative metagenomics to assemble and enumerate two Synechococcus genomes from an iron-limited, High Nutrient Low Chlorophyll region. We show these genomes represent the majority of Synechococcus cells at the site and are the first known Synechococcus unable to assimilate either nitrate or nitrite. This gene loss is likely due to the high iron quota of these proteins and predominant availability of recycled forms of nitrogen. Synechococcus loss of nitrate assimilation affects their role in elemental cycles (e.g., carbon, nitrogen, and iron), limits their potential for carbon export, and enhances our understanding of Synechococcus evolution in response to nutrient limitation and competition.