Investigation of Ciguatoxicity in Dinoflagellate Gambierdiscus and Potential Health Risks of Marine Lipophilic Phycotoxins in Coral Reef Fish

岡比亞藻的雪卡毒素毒性以及珊瑚礁魚類中海洋親脂性藻毒素的潜在健康風險研究

Student thesis: Doctoral Thesis

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Award date3 May 2024

Abstract

Marine lipophilic phycotoxins (MLPs) are natural products of toxigenic microalgae and can be accumulated within the food web, posing risks to marine organisms and human. Among the toxin-producing microalgae, dinoflagellates are the primary producers responsible for seafood poisoning syndromes. Ciguatera fish poisoning (CFP) is one of the most prominent seafood poisoning syndromes affecting millions of people globally. The dinoflagellates Gambierdiscus and Fukuyoa can produce ciguatoxins (CTXs) and maitotoxins (MTXs) that lead to CFP. In the Pacific region, the Republic of Kiribati is known as a ciguatera hotspot and one of the representative tropical small island developing states (SIDS). Due to limited resources, Kiribati heavily relies on the fisheries industry for sustenance and economic revenue. However, the country has raised seafood safety concern and experienced substantial economic losses due to CFP outbreaks.

Snappers and groupers, with high palatable and economic value, are the primary food source and fish species for exportation in Kiribati, but they are highly suspected CTX-contaminated species due to their top predatory characteristics. In our study, the level of CTXs in sixty fish specimens of snappers and groupers collected from two islands of Kiribati were analyzed by liquid chromatography-tandem mass spectrometry and cell-based assay. The results show that CTXs were detected in 74.5% of specimens from Marakei Island and 61.5% of specimens from Kiritimati Island. The highest level of CTXs (as 53-fold P-CTX-1 equivalents higher than the acute safety level) was detected in Epinephelus coeruleopunctatus collected from Marakei Island. Our findings indicated that groupers and snappers are high-risk species for ciguatera, and their export may pose health risks.

Investigation of the presence and toxicity of Gambierdiscus and Fukuyoa in Kiribati is crucial, as they are responsible for causing CFP. Previous studies reported that many strains of Gambierdiscus were isolated from Kiribati, but there is no solid evidence on the contribution of ciguatoxic strains to the incidence of CFP outbreak. In this study, toxicological assessment of Gambierdiscus and Fukuyoa was used to determine the regional risk differences of CTXs. Totally, 19 strains of Gambierdiscus and a strain of Fukuyoa from Kiribati and Malaysia were analyzed by using cytotoxicity assay of the neuro-2a cell line, hemolytic assay of fish erythrocytes, and high-resolution mass spectrometry. Gambierdiscus from Kiribati and Malaysia showed detectable ciguatoxicity. However, the Kiribati strains were more hemolytic. Putative 44-methylgambierone was identified as a contributor to the hemolytic activity, and other unknown hydrophilic toxins produced can be potentially linked to higher CFP incidence in Kiribati.

So far, most studies have focused on the detection of CTXs, a representative group of MLPs that cause ciguatera poisoning in Kiribati. However, there is still a lack of information on the contamination status of other MLPs in the region. SIDS, with their geographical isolation and limited resources, heavily rely on the fisheries industry for food and revenue. The presence of MLPs poses risks to their economy and human health. To understand the contamination status and potential risks, the Kiribati was selected as the representative tropical SIDS and 55 species of 256 coral reef fish encompassing multiple trophic levels and feeding strategies were collected to analyze 17 typical MLPs. Our results showed that the potential risks of ciguatoxins were the highest, and approximately 62% of fish species may pose risks for consumers. Biomagnification of ciguatoxins was observed in the food web, with a trophic magnification factor of 2.90. Brevetoxin-3, okadaic acid, and dinophysistoxin-1 and -2 were first reported, but the risks posed by okadaic acid and dinophysistoxins were found to be negligible. The correlation analysis revealed that fish body size or trophic position are unreliable metrics to indicate the associated risks and prevent the consumption of contaminated fish. The potential risks of MLPs in Kiribati are of concern, and our findings can serve as valuable inputs for developing food safety policies and fisheries management strategies specific to tropical SIDS contexts.