Zinc availability and alkaline phosphatase activity in Emiliania huxleyi: Implications for Zn–P co-limitation in the ocean

Zinc (Zn) serves as a cofactor in several extracellular phosphatases, which allow microorganisms to acquire phosphorus from organic P compounds. In oligotrophic ocean water, where both phosphate and Zn concentrations are low, orthophosphate regeneration through enzymatic hydrolysis of organic compounds may be restricted by Zn availability. We examined the possibility of co-limitation by P and Zn in batch cultures of the coccolithophore Emiliania huxleyi grown at very low biomass. Both growth rates and extracellular phosphatase activity were inhibited by low Zn. Cultures grown at nanomolar P and subpicomolar, unchelated Zn concentrations had higher phosphatase activity and slower growth rates when grown on organic P than when grown on inorganic P. We calculated that the additional Zn demand for phosphatase activity in the culture with organic P amounted to 16% of the cellular Zn quota. This percentage would be lower at higher organic P concentrations. Extrapolating from our data, we surmise that Zn–P co-limitation may prevail in highly oligotrophic systems such as the Sargasso Sea, but it is not likely to be widespread in the ocean. Nonetheless, the observation of a significant enhancement of extracellular phosphatase activity in Zn-amended water samples from the Bering Sea demonstrates the potential for Zn–P colimitation during phytoplankton blooms. In oligotrophic ocean regions, phytoplankton growth may be limited by low ambient inorganic phosphate concentrations (Karl and Bjorkman 2002; Lomas et al. 2004; Wu et al. 2000). To access the phosphorus contained in organic compounds (which is generally not directly available to them), phytoplankton and other microorganisms synthesize extracellular hydrolytic enzymes that cleave phosphate (PO4) from its organic moiety (Kuenzler and Perras 1965; Cambella et al. 1984). Phosphate release from a wide variety of phosphomonoesters is achieved by the activity of broad spectrum phosphatases that are commonly classified as either alkaline or acid according to their pH optima (Cambella et al. 1984). Another ectoenzyme, 59-nucleotidase, which cleaves phosphate from nucleotides, appears to be expressed 1 Corresponding author ([email protected]).