Risk of ciguatoxins is shaped by Gambierdiscus community structure

Ciguatoxins (CTXs) are produced by marine microbial eukaryotes (Gambierdiscus/Fukuyoa, Dinophyta: Alveolata) that live epiphytically on macroalgae and other substrates. When CTXs accumulate in seafood they cause Ciguatera Poisoning (CP), which affects ca. 20-50,000 people p.a. and is likely worsened by climate change. CTXs in fish are highly variable with diet, ecology, size, age and phylogeny. Chemical identification of CTXs is difficult, and while detection of Gambierdiscus is simple, often no clearly CTX-producing Gambierdiscus are known from CP sites. Here, we coupled custom deep metabarcoding with quantitative PCR, CTXs in both Gambierdiscus and a sentinel fish (Ctenochaetus striatus) with limited home range, in the Cook Islands, an endemic CP area. Using neuroblastoma cell assays and liquid chromatography-tandem mass spectrometry, CTXs were present in fish species from six families. Dinoflagellate α-diversity was dominated by nine Gambierdiscus/Fukuyoa spp., the highest diversity yet reported from a single location. Sites where the rare species, G. polynesiensis, were detected on artificial substrates and macroalgae were more closely aligned with concentrations of P-CTX3B in C. striatus, unrelated to fish age or size, than with overall Gambierdiscus abundance. Of newly isolated Gambierdiscus strains, only the three G. polynesiensis produced P-CTXs. We show rare Gambierdiscus spp. and sentinel fish can map site-specific CP risk to address a growing climate change-related public health threat.