Tissue Distribution and Metabolization of Ciguatoxins in an Herbivorous Fish following Experimental Dietary Exposure to Gambierdiscus polynesiensis

• Published in: Marine drugs Vol. 22; no. 1; p. 14
• Main Authors: Clausing, Rachel J, Ben Gharbia, Hela, Sdiri, Khalil, Sibat, Manoëlla, Rañada-Mestizo, Ma Llorina, Lavenu, Laura, Hess, Philipp, Chinain, Mireille, Bottein, Marie-Yasmine Dechraoui
• Format: Journal Article
• Language: English
• Published: Switzerland MDPI AG 01-01-2024; MDPI
• Subjects: Accumulation; Algae; Animal tissues; Bioaccumulation; Biotransformation; Carcasses; Ciguatera; ciguatera poisoning (CP); Ciguatoxin; ciguatoxins; Collections; Consumers; Dinoflagellates; Distribution; Exposure; Fish; Fish feeds; Food chains; Food matrix; Food webs; Gambierdiscus polynesiensis; Gels; Growth rate; Herbivorous fish; Herbivorous fishes; Intoxication; Invertebrates; Life Sciences; Load distribution; Marine fishes; metabolism; Microorganisms; Neurotoxins; Reef fish; Reef fishes; Risk assessment; Scale models; Seafood; Seafood safety; Seafoods; Spleen; Tissue; Toxicity; Toxins; trophic transfer; biotransformation; reef fish; liquid chromatography–tandem mass spectrometry; Gambierdiscus polynesiensis; trophic transfer; ciguatera poisoning (CP); metabolism; bioaccumulation; ciguatoxins; tissue distribution
• ISSN: 1660-3397; 1660-3397
• DOI: 10.3390/md22010014

Ciguatoxins (CTXs), potent neurotoxins produced by dinoflagellates of the genera
and
, accumulate in commonly consumed fish species, causing human ciguatera poisoning. Field collections of Pacific reef fish reveal that consumed CTXs undergo oxidative biotransformations, resulting in numerous, often toxified analogs. Following our study showing rapid CTX accumulation in flesh of an herbivorous fish, we used the same laboratory model to examine the tissue distribution and metabolization of Pacific CTXs following long-term dietary exposure.
consumed cells of
in a gel food matrix over 16 weeks at a constant dose rate of 0.36 ng CTX3C equiv g
fish d
. CTX toxicity determination of fish tissues showed CTX activity in all tissues of exposed fish (eight tissues plus the carcass), with the highest concentrations in the spleen. Muscle tissue retained the largest proportion of CTXs, with 44% of the total tissue burden. Moreover, relative to our previous study, we found that larger fish with slower growth rates assimilated a higher proportion of ingested toxin in their flesh (13% vs. 2%). Analysis of muscle extracts revealed the presence of CTX3C and CTX3B as well as a biotransformed product showing the
/
transitions of 2,3-dihydroxyCTX3C. This is the first experimental evidence of oxidative transformation of an algal CTX in a model consumer and known vector of CTX into the fish food web. These findings that the flesh intended for human consumption carries the majority of the toxin load, and that growth rates can influence the relationship between exposure and accumulation, have significant implications in risk assessment and the development of regulatory measures aimed at ensuring seafood safety.