The relationship between toxicity and mixotrophy in bloom dynamics of the ichthyotoxic Prymnesium parvum

Toxin production in planktonic protists is widespread and comprises an effective mechanism to eliminate competitors or grazers. Toxins released into the water can mediate the immobilization of prey for subsequent consumption or can mediate the lysis and uptake of the released nutrients. For the worldwide-distributed ichthyotoxic and mixotrophic haptophyte Prymnesium parvum, the relationship between toxin production; impact on co-occurring species, and mixotrophy remains blurred. In the current study, we show that changes in salinities (5 vs 30), phosphorous (P) availabilities (P-replete vs P-deplete) and cell densities affect growth, toxicity and mixotrophy in P. parvum. Cell density positively affected cellular toxin content by a factor of up to 10. Low salinity resulted in a higher mortality of the cryptophyte prey Teleaulax acuta, with ~80% of cells being lysed after 2 h of incubation. However, phagotrophic rates were higher in P-deplete conditions, independent of the salinity. Transcriptomic analysis of the monocultures revealed the up-regulation of genes involved in endocytosis under either low salinity and phosphorous, suggesting that this process is evolutionarily conserved, triggered by environmental stressors and independent of prey presence. Polyketide synthase genes, potentially involved in toxin biosynthesis, exhibited distinct expression patterns, depending on the physiological status, toxicity and with generally higher expression under the high cell density conditions. Overall, our study contributes to a better understanding of the dynamics between the two critical processes of toxin production and mixotrophy, and has important implications for bloom formation and its maintenance in this ecologically important species.