Nutrient limitation determines biological interactions between a mixotrophic Chrysophyte and toxin-producing Microcystis

Abstract

Blooms of toxigenic cyanobacteria pose a mounting risk to aquatic ecosystems. Relative to abiotic drivers of cyanobacteria success, biotic processes have received less attention. Mixotrophic nanoflagellates that combine heterotrophic ingestion of particulate prey with photoautotrophy are among the eukaryotes that can resist cyanotoxins. We used laboratory experiments in culture to integrate top-down (herbivory) and bottom-up (nitrogen and phosphorus limitation) controls on the growth and production of microcystin-LR, including biodegradation products, of Microcystis by Ochromonas (mixotroph) and Spumella (heterotroph). A notable reduction in the growth rate of toxic Microcystis was evident in co-culture with either Ochromonas or Spumella under P-limitation. Under P-limitation, the co-culture of toxic Microcystis with Ochromonas also led to a reduction in concentration of microcystin-LR (MC-LR and an increase in biodegradation products. Grazing rates up to 31 and 50 cell−1 day−1 on toxic Microcystis were recorded for Ochromonas and Spumella, respectively. The highest grazing rates by Ochromonas were observed on toxic Microcystis under N-limitation. Hence, it is likely that Ochromonas is an herbivore of toxic Microcystis under N-limitation and a competitor for nutrients under P-limitation. Collectively, these results suggest a role of eukaryotic nanoflagellates in decreasing the biomass and toxicity associated with cyanobacteria blooms that vary with nutrient availability.