Ciguatoxicity of Gambierdiscus and Fukuyoa species from the Caribbean and Gulf of Mexico

Type Article
Date 2017-10
Language English
Author(s) Litaker R. Wayne1, Holland William C.1, Hardison D. Ransom1, Pisapia Francesco2, Hess PhilippORCID2, Kibler Steven R.1, Tester Patricia A.3
Affiliation(s) 1 : Natl Ocean Serv, Natl Ctr Coastal Ocean Sci, Ctr Coastal Fisheries & Habitat Res, Beaufort, NC 28516 USA.
2 : Inst Francais Rech Exploitat Mer, Lab Phycotoxines, Nantes, France.
3 : Ocean Tester LLC, Beaufort, NC USA.
Source Plos One (1932-6203) (Public Library Science), 2017-10 , Vol. 12 , N. 10 , P. e0185776 (1-19)
DOI 10.1371/journal.pone.0185776
WOS© Times Cited 27
Abstract

Dinoflagellate species belonging to the genera Gambierdiscus and Fukuyoa produce ciguatoxins (CTXs), potent neurotoxins that concentrate in fish causing ciguatera fish poisoning (CFP) in humans. While the structures and toxicities of ciguatoxins isolated from fish in the Pacific and Caribbean are known, there are few data on the variation in toxicity between and among species of Gambierdiscus and Fukuyoa. Quantifying the differences in species-specific toxicity is especially important to developing an effective cell-based risk assessment strategy for CFP. This study analyzed the ciguatoxicity of 33 strains representing seven Gambierdiscus and one Fukuyoa species using a cell based Neuro-2a cytotoxicity assay. All strains were isolated from either the Caribbean or Gulf of Mexico. The average toxicity of each species was inversely proportional to growth rate, suggesting an evolutionary trade-off between an investment in growth versus the production of defensive compounds. While there is 2- to 27-fold variation in toxicity within species, there was a 1740-fold difference between the least and most toxic species. Consequently, production of CTX or CTX-like compounds is more dependent on the species present than on the random occurrence of high or low toxicity strains. Seven of the eight species tested (G. belizeanus, G. caribaeus, G. carolinianus, G. carpenteri, Gambierdiscus ribotype 2, G. silvae and F. ruetzleri) exhibited low toxicities, ranging from 0 to 24.5 fg CTX3C equivalents cell-1, relative to G. excentricus, which had a toxicity of 469 fg CTX3C eq. cell-1. Isolates of G. excentricus from other regions have shown similarly high toxicities. If the hypothesis that G. excentricus is the primary source of ciguatoxins in the Atlantic is confirmed, it should be possible to identify areas where CFP risk is greatest by monitoring only G. excentricus abundance using species-specific molecular assays.

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Publisher's official version 19 1 MB Open access
S1 Fig. Ciguatoxicity versus growth rate plotted on a linear scale. 898 KB Open access
S1 Table. Comprehensive table showing what is known about CTX and MTX production by Gambierdiscus and Fukuyoa isolates not included in this study. 43 597 KB Open access
S2 Table. Comparison of the Gambierdiscus and Fukuyoa growth rate estimates determined in this study versus rates published in other studies. 3 168 KB Open access
S3 Table. A. Ratio of the highest toxicity isolate divided by the lowest isolate in fg CTX3C eq. cell-1. 1 94 KB Open access
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