Proteomic and biogeochemical perspectives on cyanobacteria nutrient acquisition-Part 1: Zonal gradients in phosphorus and nitrogen acquisition and stress revealed by metaproteomes of Prochlorococcus and Synechococcus

Abstract

Ocean productivity is maintained by key nutrients, including nitrogen, phosphorus and trace metals. The magnitude and stoichiometry of nutrient fluxes to the ocean is changing. Here, we investigate how natural assemblages of marine microbes in the subtropical North Atlantic respond to variation in nutrient availability along a natural zonal gradient. We measure dissolved nutrient concentrations, biological rates, and characterize the microbial proteomes of the dominant picocyanobacteria, Prochlorococcus and Synechococcus. Moving west to east, dissolved organic phosphorus (DOP) and phosphate concentrations increased, and dissolved iron decreased. Prochlorococcus abundance increased eastwards, whereas Synechococcus abundance was highest in the west. Zonal distributions of protein biomarkers representing phosphorus (PstS, PhoA, PhoX), nitrogen (P-II, UrtA, AmtB) and trace metal metabolism (related to iron, zinc and cobalt) from metaproteomes, together with rates of alkaline phosphatase activity, indicate greater phosphorus stress in the west than the east for both picocyanobacteria. In the east, elevated levels of protein biomarkers for nitrogen, iron, zinc and cobalamin in Prochlorococcus indicate a transition to nitrogen stress and greater influence of trace metal resources. Measured responses of Prochlorococcus ecotypes and Synechococcus clades to DOP, iron and zinc additions in incubation experiments further indicate divergent regulation in uptake and acquisition of phosphorus by these picocyanobacteria across the transect, albeit with caveats on the potential for differences in regulation within a genus and between strains. Together our findings suggest a basin-scale transition from phosphorus stress in picocyanobacteria in the west to nitrogen stress in the east.