Nutrient and Trace Metal Controls on Alkaline Phosphatase in the Subtropical Ocean: Insights from Bioassays and Gene Expression

Phosphorus is an essential nutrient for all life on earth. In the ocean, the most bioavailable form of phosphorus is inorganic phosphate, but in the extensive subtropical gyres, phosphate concentrations can be chronically low in the surface ocean and limit biological activity. In response to phosphate limitation, organisms produce phosphohydrolytic enzymes, such as alkaline phosphatases (AP), that enable them to utilize the more replete dissolved organic phosphorus (DOP) pool to meet their cellular phosphorus demands. Synthesis of data from the surface ocean from 14 open ocean studies reveals an inverse hyperbolic relationship between phosphate and AP, where AP is significantly induced at phosphate concentrations below 50 nM and DOP concentrations decrease as AP increases. AP activity was significantly higher in the subtropical Atlantic compared to the subtropical Pacific Ocean, even over the same low phosphate concentration range (0 to 50 nM). While the phosphate concentration may have a first order control on the rates of AP, we demonstrate that other factors influence AP activity. AP are metalloenzymes and zinc and iron are co-factors of the AP proteins PhoA and PhoX, respectively. Using bioassay experiments, we show that the addition of Saharan dust and zinc significantly increases the rate of AP. To our knowledge, our results are the first direct field-based evidence that AP activity is limited by zinc in the subtropical ocean. In colonies of nitrogen fixer, Trichodesmium, we found enhanced expression of the phoA gene in a region of elevated zinc concentrations and enhanced expression of the phoX gene in a region of elevated iron concentrations around the intertropical convergence zone. Our study highlights the potential link between the phosphorus cycle and trace metals, specifically zinc and iron, and implies that there is potential for zinc-phosphorus and iron-phosphorus co-limitation in the ocean via AP.