Differential effects of phosphorus limitation on cellular metals in Chlorella and Microcystis
Limnol. Oceanogr., 53(5), 2008, 1790-1804 | DOI: 10.4319/lo.2008.53.5.1790
ABSTRACT: We investigated the effect of phosphate bioavailability on cellular metal quotas in two species of freshwater phytoplankton (the eukaryote Chlorella sp. UTCC522 and the cyanobacterium Microcystis sp. LE3), grown in semicontinuous culture over four controlled levels of phosphate availability, encompassing phosphorus (P) deplete to P replete conditions. P limitation caused reduced growth rate, high C: P (up to 1800 mol mol-1), and increased alkaline phosphatase (APase) activity. Low P availability led to enriched cobalt (Co), cadmium (Cd), and zinc (Zn) in Chlorella (up to 2.8-fold, 1.7-fold, and 1.8-fold, respectively, normalized to cellular N, relative to P-replete control) but resulted in enriched Co and nickel (Ni) in Microcystis (up to 4.4-fold and 3.0-fold). In contrast, cellular iron (Fe), manganese (Mn) and copper (Cu) were largely unchanged (±~20%) in both organisms. Cd and Co may substitute for Zn in the APase of Chlorella while in Microcystis the dominant phosphatase may be strictly Co-requiring, as has been reported for other prokaryotes and is consistent with its evolutionary emergence before the oxygenation of the atmosphere, when Co was relatively abundant in natural waters. By extension, the absolute Co requirement of the important marine cyanobacteria Synechococus and Prochlorococcus may be related in part to widespread depletion of orthophosphate (PO43-) in the oligotrophic surface ocean. The enrichment of Ni in Microcystis may indicate increased activity of Ni-requiring superoxide dismutase under P limitation or, speculatively, a co-uptake of Ni and Co by a shared transport system. These results shed light on the interaction between trace metals, macronutrient availability, and phytoplankton assemblage composition, and suggest intensified biological cycling of Zn, Cd, Co, and Ni in low-P freshwater and marine systems.