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

Type Article
Date 2024-01
Language English
Author(s) Clausing Rachel J.ORCID1, 2, Ben Gharbia HelaORCID3, Sdiri Khalil3, Sibat ManoellaORCID4, Rañada-Mestizo Ma. Llorina5, Lavenu Laura3, Hess PhilippORCID4, Chinain MireilleORCID6, Bottein Marie-Yasmine DechraouiORCID7
Affiliation(s) 1 : Dipartimento di Scienze della Terra dell’Ambiente e della Vita, Università degli Studi di Genova, 16132 Genova, Italy
2 : Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA
3 : IAEA Marine Environment Laboratories, International Atomic Energy Agency, 98000 Monaco, Monaco
4 : Ifremer, ODE/PHYTOX/METALG, Rue de l’île d’Yeu, F-44300 Nantes, France
5 : IAEA Collaborating Center on Harmful Algal Bloom (HAB) Studies, Chemistry Research Section, Department of Science and Technology, Philippine Nuclear Research Institute (DOST-PNRI), Diliman, Quezon City 1101, Philippines
6 : Laboratoire des Biotoxines Marines, UMR 241 EIO, Institut Louis Malardé, BP 30, Papeete-Tahiti 98713, French Polynesia
7 : Université Côte d’Azur, CNRS, ECOSEAS, UMR7035, Parc Valrose, CEDEX 2, 06103 Nice, France
Source Marine Drugs (1660-3397) (MDPI AG), 2024-01 , Vol. 22 , N. 1 , P. 14 (22p.)
DOI 10.3390/md22010014
Note This article belongs to the Special Issue Marine Biotoxins 3.0
Keyword(s) ciguatoxins, ciguatera poisoning (CP), trophic transfer, metabolism, biotransformation, bioaccumulation, tissue distribution, Gambierdiscus polynesiensis, reef fish, liquid chromatography-tandem mass spectrometry

Ciguatoxins (CTXs), potent neurotoxins produced by dinoflagellates of the genera Gambierdiscus and Fukuyoa, 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. Naso brevirostris consumed cells of Gambierdiscus polynesiensis in a gel food matrix over 16 weeks at a constant dose rate of 0.36 ng CTX3C equiv g−1 fish d−1. 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 m/z 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.

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Clausing Rachel J., Ben Gharbia Hela, Sdiri Khalil, Sibat Manoella, Rañada-Mestizo Ma. Llorina, Lavenu Laura, Hess Philipp, Chinain Mireille, Bottein Marie-Yasmine Dechraoui (2024). Tissue Distribution and Metabolization of Ciguatoxins in an Herbivorous Fish following Experimental Dietary Exposure to Gambierdiscus polynesiensis. Marine Drugs, 22(1), 14 (22p.). Publisher's official version : https://doi.org/10.3390/md22010014 , Open Access version : https://archimer.ifremer.fr/doc/00868/98004/