Paralytic Shellfish Toxin production in Alexandrium minutum (Dinophyceae): insights from omics integration using toxigenic and non-toxigenic recombinant progeny

Paralytic Shellfish Toxins (PSTs) are produced by certain species of cyanobacteria and dinoflagellates. Part of the PST biosynthetic pathway has been elucidated in cyanobacteria, and the implication of some sxt genes has been confirmed by experimental studies. Contrary to cyanobacteria, knowledge about PST biosynthesis in dinoflagellates is more limited and generally restricted to comparative studies with the cyanobacterial pathway. To investigate the specificity of the PST pathway in dinoflagellates, 16 toxic and non-toxic A. minutum strains from a recombinant cross were compared, without prior assumption on genes or metabolites involved in PST synthesis, using an integrative approach combining untargeted metabolomic and transcriptomic data. Among the 60 most distinguishing transcripts between toxic and non-toxic strains, only 3 sxt genes were present, sxtA4, sxtG, and sxtI. In contrast, non-sxt homologs were detected as highly discriminant between these two phenotypes. More specifically, a phyH homolog may act as the analog of sxtS found in cyanobacteria. Moreover, we identified four putative synthetic PST intermediates. Among these, Int-C2, correlated with the toxic phenotype, whereas 3 others were detected in both toxic and non-toxic strains, suggesting that these strains may share some parts of the biosynthetic pathway. Finally, our results showed that PST biosynthesis in dinoflagellate results from the activity of sxt genes, acquired by horizontal gene transfer from cyanobacteria, as well as from other genes not acquired from cyanobacteria, such as phyH.