Part 1: Zonal gradients in phosphorus and nitrogen acquisition and stress revealed by metaproteomes of Prochlorococcus and Synechococcus

Abstract. Ocean warming alongside changes to the natural and anthropogenic supply of key nutrient resources such as nitrogen, phosphorus and trace metals is predicted to alter the magnitude and stoichiometry of nutrients that are essential for maintaining ocean productivity. To improve our ability to predict how marine microbes will respond to a changing nutrient environment, we need to better understand how natural assemblages of marine microbes acquire nutrients. We combined observations of natural zonal gradients across the North Atlantic subtropical gyre of the state of nutrient resources and microbial proteomes with biological activity rates, to investigate the factors influencing the distributions and nutrient acquisition strategies of the dominant picocyanobacteria, Prochlorococcus and Synechococcus. Dissolved organic phosphorus decreased by more than a factor of two moving westward, while phosphate increased eastward with eastern boundary upwelling and dissolved iron increased westward with dust deposition. Picocyanobacterial populations diverged across the zonal transect with Prochlorococcus increasing in abundance westward, while maintaining numerical dominance throughout, and while Synechococcus increased in abundance in the westward basin, implying a low phosphorus niche. We analysed the zonal distribution of protein biomarkers representing phosphorus (PstS, PhoA, PhoX), nitrogen (P-II, UrtA, AmtB) and trace metal metabolism (related to iron, zinc and cobalt) alongside the response of phosphorus protein biomarkers to the addition of dissolved organic phosphorus with iron or zinc within incubation experiments. Rates of alkaline phosphatase alongside phosphorus protein biomarkers concur on more intense phosphorus stress in the western compared to the eastern subtropical Atlantic for both picocyanobacteria. Protein biomarkers for nitrogen, iron, zinc and cobalamin in Prochlorococcus increased to the east where phosphorus protein biomarkers were lower, indicating a transition to N stress and increasing role of trace metal resources in controlling Prochlorococcus growth. We use the diverging zonal patters in protein biomarkers, alongside the response of Prochlorococcus and Synechococcus to nutrient addition, to provide insight into the environmental controls on protein biomarkers of picocyanobacteria across the subtropical gyre. For example, the addition of DOP, Fe or Zn decreased PstS and PhoA in Prochlorococcus but increased PstS and PhoA in Synechococcus, implying divergence in regulation of phosphorus uptake or acquisition strategy. We postulate on the coinciding influences of upwelling, nitrogen fixation and atmospheric deposition on nutrient resources and controlling biogeography of picocyanobacteria. Together these biogeochemical and metaproteomic data imply a basin-scale transition from phosphorus stress in the west to nitrogen stress in the east within the picocyanobacteria on this zonal transect across the North Atlantic Ocean, with implications for productivity.