High-resolution multiomics links nutrients and mixotrophy to toxicity in a harmful bloom of the haptophyte Chrysochromulina leadbeateri

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Harmful algal blooms (HABs) of the toxigenic haptophyte Chrysochromulina are known to cause fish mortalities and collateral ecosystem damage. The ichthyotoxic mechanisms are poorly understood but likely dependent on toxigenesis by polyketide synthases (PKSs). We hypothesize that induction of PKS activity facilitates mixotrophic behavior during nutrient-depleted bloom conditions. To identify potential in situ stimuli for growth, toxigenicity, and bloom persistence, we compared environmental factors and biological processes identified by metaomics to Chrysochromulina leadbeateri HABs between two fjords in northern Norway. We identified the polyketide ichthyotoxin leadbeaterin-1 from the C. leadbeateri bloom and found potentially associated candidate PKS genes of which most were higher expressed at bloom stations. A relative depletion of inorganic nitrogen and phosphate during the bloom was correlated with higher expression of genes involved in endocytosis, autophagy, and lysosomal activity. Mixotrophy is evidently a compensatory nutritional strategy coupled to induction of toxigenesis and other metabolomic processes as biotic factors linked to Chrysochromulina bloom dynamics.

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