Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake

We investigated the dynamics and toxicity of cyanobacteria populations in Lake Agawam, a eutrophic New York lake, and concurrently conducted experiments to evaluate the contrasting effects of zooplankton (mesozooplankton and microzooplankton) grazing and nutrient loading on the abundance and toxin content of cyanobacteria populations. Molecular techniques were used to assess the presence and expression of the microcystin synthetase gene. Lake Agawam hosted dense blooms (>10⁵ cells mL^-1) of Microcystis sp. and Anabaena sp. with consistently elevated levels of microcystin (1.0-25 μg L^-1) and lower levels of anatoxin-a (∼1.0 μg L^-1 during late summer only). Polymerase chain reaction (PCR) analysis targeting the microcystin synthetase gene (mcyE) indicated that Microcystis sp., and not Anabaena sp., was responsible for microcystin production in this system. Moreover, reverse transcriptase PCR (RT-PCR) indicated that the Microcystis population expressed the mcyE gene during summer months, but that gene expression declined to undetectable levels during the fall as in situ cell densities in the lake declined. During summer, when there was elevated Microcystis densities (>8 × 10⁴ cells mL^-1) expressing mcyE, experimental Daphnia sp. enrichment did not alter algal biomass (100% of experiments; n = 6). However, during fall months when the mcyE gene expression was not detected and Microcystis densities were lower and declining (4 × 10³ to 5 × 10⁴ cells mL^-1), zooplankton enrichment yielded significantly reduced (p < 0.05) cyanobacteria biomass relative to control treatments in most experiments (80%; n = 4). In contrast to mesozooplankton, microzooplankton actively grazed algal biomass at significant rates (1.2 ± 0.3 day^-1) throughout the study. Microcystis and other cyanobacterial populations did not respond to nutrient amendments during early summer but experienced significantly increased growth rates and toxin concentrations (microcystin and anatoxin-a) during late summer and early fall nitrogen enrichment experiments. As such, the dominance of Microcystis sp. blooms during the summer was linked to nutrient replete conditions and the suppression of mesozooplankton (but not microzooplankton) grazing which itself appeared to be influenced by cellular toxin synthesis by Microcystis. The demise of the bloom was associated with N-limitation which reduced growth rates and toxin production by Microcystis and in turn may have permitted zooplankton to graze cells.