Use of Mass Spectrometry to Determine the Diversity of Toxins Produced by Gambierdiscus and Fukuyoa Species from Balearic Islands and Crete (Mediterranean Sea) and the Canary Islands (Northeast Atlantic)

Abstract

Over the last decade, knowledge has significantly increased on the taxonomic identity and distribution of dinoflagellates of the genera Gambierdiscus and Fukuyoa. Additionally, a number of hitherto unknown bioactive metabolites have been described, while the role of these compounds in ciguatera poisoning (CP) remains to be clarified. Ciguatoxins and maitotoxins are very toxic compounds produced by these dinoflagellates and have been described since the 1980s. Ciguatoxins are generally described as the main contributors to this food intoxication. Recent reports of CP in temperate waters of the Canary Islands (Spain) and the Madeira archipelago (Portugal) triggered the need for isolation and cultivation of dinoflagellates from these areas, and their taxonomic and toxicological characterization. Maitotoxins, and specifically maitotoxin-4, has been described as one of the most toxic compounds produced by these dinoflagellates (e.g., G. excentricus) in the Canary Islands. Thus, characterization of toxin profiles of Gambierdiscus species from adjacent regions appears critical. The combination of liquid chromatography coupled to either low- or high-resolution mass spectrometry allowed for characterization of several strains of Gambierdiscus and Fukuyoa from the Mediterranean Sea and the Canary Islands. Maitotoxin-3, two analogues tentatively identified as gambieric acid C and D, a putative gambierone analogue and a putative gambieroxide were detected in all G. australes strains from Menorca and Mallorca (Balearic Islands, Spain) while only maitotoxin-3 was present in an F. paulensis strain of the same region. An unidentified Gambierdiscus species (Gambierdiscus sp.2) from Crete (Greece) showed a different toxin profile, detecting both maitotoxin-3 and gambierone, while the availability of a G. excentricus strain from the Canary Islands (Spain) confirmed the presence of maitotoxin-4 in this species. Overall, this study shows that toxin profiles not only appear to be species-specific but probably also specific to larger geographic regions.

Effects of synthetic ciguatoxin CTX3C and 44-methylgambierone (MTX3) on voltage-gated sodium channels and their in vivo toxicity

“…Blooms of these dinoflagellates have expanded worldwide reaching even European coasts. In fact, the presence of Gambierdiscus species and the related toxins and CFP intoxications have been repeatedly identified in Europe during the last decades, especially in the Canary Islands [1,2] and Madeira [3]. Besides ciguatoxins, which can cause long term neurological complications in humans as a consequence of their permanent activation voltage-gated sodium channels [4][5][6], the structure of an additional ciguatoxin-related toxin named 44-methylgambierone (MTX3) has been recently elucidated [7].…”

Critical Review and Conceptual and Quantitative Models for the Transfer and Depuration of Ciguatoxins in Fishes

“…The structure of MTX-3 was recently suggested to be 44-methylgambierone [ 57 , 58 ], and has been detected in many Gambierdiscus and Fukuyoa species [ 59 , 60 , 61 , 62 , 63 , 64 ]. However, Murray et al [ 62 ] reported the toxicity (LD 50 ) of 44-methylgambierone injected intraperitoneally (i.p.)…”

Ciguatera Mini Review: 21st Century Environmental Challenges and the Interdisciplinary Research Efforts Rising to Meet Them

“…These factors include physical oceanographic properties (e.g., irradiance, wave power, depth, salinity, and temperature), biological (predation, direct and indirect disturbances), and anthropogenic drivers (habitat modification, pollution, and fishing practices) [ 10 , 15 , 98 , 99 , 100 , 101 , 102 , 103 ]. In culture, Gambierdiscus has displayed inter- and intra-species variability for growth, morphology, and quali-quantitative toxin profile [ 83 , 104 ], which can be influenced by capture location, culture parameters, and time spent in culture (phycological drift) [ 20 , 73 , 74 , 75 , 104 , 105 , 106 , 107 , 108 ]. Interactions between bacterial or other microbial co-inhabitants and Gambierdiscus indicated antagonism, competition, or benefits with impacts on fitness and bi-directional regulation in compound production [ 109 , 110 , 111 ].…”