Nutrient pulse induces dynamic changes in cellular C:N:P, amino acids, and paralytic shellfish poisoning toxins in Alexandrium tamarense

Alexandrium tamarense is a common harmful algal bloom species that can cause high concentrations of paralytic shellfish poisoning toxins (PSTs) in marine coastal waters. PSTs are nitrogen-rich alkaloids, and their production has been shown to depend on resource conditions as well as on growth rate. We hypothesized that PST content in A. tamarense depends on the nitrogen availability and will increase with cellular N: P ratios and arginine content. To test this hypothesis, we first grew A. tamarense cells under nitrogen-starved, phosphorus-starved and nutrient-replete conditions. Subsequently, we transferred cells into a nutrient-rich medium and followed dynamic changes in growth, elemental stoichiometry, as well as amino acid and PST content and composition. Our results illustrate that PST content was lowest under nitrogen starvation, intermediate under nutrient-replete conditions, and highest under phosphorus starvation. As expected, PST content correlated well with cellular N: P ratios and arginine content. Upon transfer of cells into a nutrient-replete medium, PST content varied with growth rate, depending on the growth-controlling resource. Specifically, PST content increased with growth when recovering from nitrogen starvation and decreased with growth when recovering from phosphorus starvation. Furthermore, PST composition shifted towards less hydroxylated analogues upon resumption of growth. Our findings also illustrate a high potential for luxury consumption of phosphorus by A. tamarense. The applied comprehensive approach will help to further elucidate the intriguing coupling between carbon, nitrogen and phosphorus assimilation and the synthesis of amino acids and PSTs.