Morphology, phylogeny, and toxicity of three Gambierdiscus species from the South China Sea, including a coral-killing bloom of G. carpenteri in reef tanks

Abstract

Gambierdiscus is a genus of benthic dinoflagellate commonly found in coral reef ecosystems. Some species produce neurotoxins, such as ciguatoxins (CTXs) and maitotoxins (MTXs), which have been linked to ciguatera poisoning (CP), an illness prevalent in tropical regions. In this study, three Gambierdiscus species, G. caribaeus, G. carpenteri, and G. vietnamensis were identified from coral reefs of the South China Sea based on detailed morphological and phylogenetic analyses. This is the first report of G. carpenteri along the Chinese coast, and a bloom of G. carpenteri in coral culture tank that caused coral mortality was documented. While no known CTXs and MTXs were detected in the newly isolated Gambierdiscus strains, 44-methylgambierone was present in all three species; further, G. carpenteri strains produced protonated adducts of Gambieric acids A and C. The results of MTT in vitro assay showed that G. vietnamensis exhibited the highest cytotoxicity to both cancerous and noncancerous cell lines, while G. caribaeus demonstrated moderate inhibition of noncancerous cells and colon adenocarcinoma, with lower toxicity against other colon cancer cell lines. In contrast, the bloom samples of G. carpenteri showed low cytotoxicity across all tested cell lines, suggesting that G. carpenteri may affect coral health through mechanisms beyond cytotoxicity. Higher nitrogen levels relative to phosphorus likely promoted the initiation of G. carpenteri blooms and sustained the high density in the culture tanks. The shading effect by the massive G. carpenteri mats likely limited the light intensity required by the corals, while elevated NH₄⁺-N concentrations during the bloom period may further contribute to coral mortality. These findings underscore the effects of Gambierdiscus species influencing coral health, highlighting the need for further investigation into the mechanisms underlying the impacts on the reef ecosystems.