Differentiating toxic and nontoxic congeneric harmful algae using the non-polar metabolome

Recognition and rejection of chemically defended prey is critical to maximizing fitness for predators. Paralytic shellfish toxins (PSTs) which strongly inhibit voltage-gated sodium channels in diverse animal taxa are produced by several species of the bloom-forming algal genus Alexandrium where they appear to function as chemical defenses against grazing copepods. Despite PSTs being produced and localized within phytoplankton cells, some copepods distinguish toxic from non-toxic prey, selectively ingesting less toxic cells, in ways that suggest cell surface recognition perhaps associated with non-polar metabolites. In this study LC/MS and NMR-based metabolomics revealed that the non-polar metabolomes of two toxic species (Alexandrium catenella and Alexandrium pacificum) vary considerably from their non-toxic congener Alexandrium tamarense despite all three being very closely related. Toxic and non-toxic Alexandrium spp. were distinguished from each other by metabolites belonging to seven lipid classes. Of these, 17 specific metabolites were significantly more abundant in both toxic A. catenella and A. pacificum compared to non-toxic A. tamarense suggesting that just a small portion of the observed metabolic variability is associated with toxicity. Future experiments aimed at deciphering chemoreception mechanisms of copepod perception of Alexandrium toxicity should consider these metabolites, and the broader lipid classes phosphatidylcholines and sterols, as potential candidate cues.

Automated summary

Traditionally, copepods have been thought to distinguish toxic from non-toxic prey by associating cell surface recognition with non-polar metabolites. LC/MS and NMR analysis revealed significant differences in the non-polar metabolomes of toxic Alexandrium species compared to their non-toxic counterparts, particularly in metabolites belonging to seven lipid classes.