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Toxicity Screening of a Gambierdiscus Australes Strain from the Western Mediterranean Sea and Identification of a Novel Maitotoxin Analogue

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Toxicity Screening of a Gambierdiscus Australes Strain from the Western Mediterranean Sea and Identification of a Novel Maitotoxin Analogue marine drugs Article Toxicity Screening of a Gambierdiscus australes Strain from the Western Mediterranean Sea and Identification of a Novel Maitotoxin Analogue Pablo Estevez 1 , David Castro 1, José Manuel Leão-Martins 1 , Manoëlla Sibat 2 , Angels Tudó 3 , Robert Dickey 4, Jorge Diogene 3 , Philipp Hess 2 and Ana Gago-Martinez 1,* 1 Biomedical Research Centre (CINBIO), Department of Analytical and Food Chemistry, University of Vigo, Campus Universitario de Vigo, 36310 Vigo, Spain; [email protected] (P.E.); [email protected] (D.C.); [email protected] (J.M.L.-M.) 2 Laboratoire Phycotoxines, Ifremer, Rue de l’Île d’Yeu, 44311 Nantes, France; [email protected] (M.S.); [email protected] (P.H.) 3 Marine and Continental Waters Programme, Institut de Recerca i Tecnologies Agroalimentàries (IRTA), Ctra. Poble Nou, km. 5.5, 43540 Sant Carles de la Ràpita, Spain; [email protected] (A.T.); [email protected] (J.D.) 4 Department of Marine Science, Marine Science Institute, University of Texas at Austin, Port Aransas, TX 78373, USA; [email protected] * Correspondence: [email protected]; Tel.: +34-64-734-3417 Abstract: Dinoflagellate species of the genera Gambierdiscus and Fukuyoa are known to produce ciguatera poisoning-associated toxic compounds, such as ciguatoxins, or other toxins, such as Citation: Estevez, P.; Castro, D.; maitotoxins. However, many species and strains remain poorly characterized in areas where they Leão-Martins, J.M.; Sibat, M.; Tudó, were recently identified, such as the western Mediterranean Sea. In previous studies carried out by A.; Dickey, R.; Diogene, J.; Hess, P.; our research group, a G. australes strain from the Balearic Islands (Mediterranean Sea) presenting Gago-Martinez, A. Toxicity Screening MTX-like activity was characterized by LC-MS/MS and LC-HRMS detecting 44-methyl gambierone of a Gambierdiscus australes Strain and gambieric acids C and D. However, MTX1, which is typically found in some G. australes strains from the Western Mediterranean Sea from the Pacific Ocean, was not detected. Therefore, this study focuses on the identification of and Identification of a Novel G. australes Maitotoxin Analogue. Mar. Drugs the compound responsible for the MTX-like toxicity in this strain. The strain was 2021, 19, 460. https://doi.org/ characterized not only using LC-MS instruments but also N2a-guided HPLC fractionation. Following 10.3390/md19080460 this approach, several toxic compounds were identified in three fractions by LC-MS/MS and HRMS. A novel MTX analogue, named MTX5, was identified in the most toxic fraction, and 44-methyl Academic Editor: Pedro Reis Costa gambierone and gambieric acids C and D contributed to the toxicity observed in other fractions of this strain. Thus, G. australes from the Mediterranean Sea produces MTX5 instead of MTX1 in Received: 14 July 2021 contrast to some strains of the same species from the Pacific Ocean. No CTX precursors were detected, Accepted: 13 August 2021 reinforcing the complexity of the identification of CTXs precursors in these regions. Published: 15 August 2021 Keywords: N2a; LC-MS/MS; LC-HRMS; maitotoxin; ciguatoxin; ciguatera poisoning Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Species of dinoflagellates of the genera Gambierdiscus and Fukuyoa are known to produce toxic metabolites [1]. Ciguatoxins (CTXs) and maitotoxins (MTXs) are included among these toxic compounds, as are some other non-structurally-related cyclic polyethers, Copyright: © 2021 by the authors. such as gambierol, gambieroxide, gambierone and gambieric acids [2–6]. Licensee MDPI, Basel, Switzerland. CTXs are cyclic polyethers of around 1100 Da and considered the main compounds re- This article is an open access article sponsible for ciguatera poisoning (CP) due to their lipophilic nature and their accumulation distributed under the terms and in fish tissue [7]. Depending on their structural differences, CTXs are classified as P-CTXs, conditions of the Creative Commons Attribution (CC BY) license (https:// C-CTXs or I-CTXs [8–10]. The algal precursors of P-CTXs were identified in dinoflagellate creativecommons.org/licenses/by/ cultures from the Pacific Ocean, being oxidized when accumulated in fish [11]. In contrast, 4.0/). CTX precursors were not identified in dinoflagellate cultures from the Indian or Atlantic Mar. Drugs 2021, 19, 460. https://doi.org/10.3390/md19080460 https://www.mdpi.com/journal/marinedrugs Mar. Drugs 2021, 19, x 2 of 20 Mar. Drugs 2021, 19, 460 2 of 19 [11]. In contrast, CTX precursors were not identified in dinoflagellate cultures from the oceans,Indian includingor Atlantic the oceans, Caribbean including Sea, thereby the Caribbean limiting Sea, the detectionthereby limiting of C-CTXs the anddetection I-CTXs of toC- theirCTXs oxidized and I-CTXs forms to intheir fish oxidized tissues. C-CTXs,forms in endemicfish tissue ins. theC-CTXs, Caribbean endemic Sea, in and the a Carib- wide varietybean Sea, of differentand a wide dinoflagellate variety of different species, weredinofla recentlygellate identifiedspecies, were and recently confirmed identified in fish andand watersconfirmed from in the fish western and waters Atlantic from Ocean, the western mainly nearAtlantic the CanaryOcean, Islandsmainly (Spain)near the and Ca- Madeiranary Islands archipelago (Spain) and (Portugal), Madeira which archipelago are therefore (Portugal), considered which are emerging therefore areas considered for the occurrenceemerging areas of CP for [12 the–15 occurrence]. of CP [12–15]. MTXsMTXs areare considered the the most most toxic toxic marine marine biotoxins biotoxins identified identified to date to date [16]. [ 16Six]. MTX Six MTXanalogues analogues have have been been identified identified to todate: date: maitotoxin maitotoxin-1-1 (MTX1), (MTX1), maitotoxin-2maitotoxin-2 (MTX2),(MTX2), maitotoxin-3maitotoxin-3 (44-methyl (44-methyl gambierone), gambierone), maitotoxin-4 maitotoxin (MTX4),-4 (MTX4), desulfo-MTX1 desulfo-MTX1 and and didehydro- didehy- demethyl-desulfo-MTX1dro-demethyl-desulfo-MTX1 (Figure (Figure1). All 1) MTXs. All MTXs are characterized are characterized structurally structurally by having by hav- at leasting at one least sulfate one group,sulfate givinggroup, themgiving increased them increased polarity polarity compared compared to CTXs. to Their CTXs. higher Their polarityhigher polarity limits their limit absorptions their absorption when ingested, when ingested leading, toleading them to not them being not considered being consid- the mainered compoundsthe main compounds responsible responsible for CP, despite for CP the, despite presence the of presence reports that of reports suggest that their suggest accu- mulationtheir accumulation in fish tissues in fish [17]. tissue MTXs analogues [17]. MTX are analogues large natural are large non-polymeric natural non compounds-polymeric aroundcompounds 3300–3400 around Da 330 in size0–3400 [18– Da21]. in MTX1 size [18 and–21]. MTX4 MTX1 have and been MTX4 associated have been with associated massive calciumwith a massive influx in calcium cells, causing influx in mortality. cells, causing MTX2 mortality. was isolated MTX2 in thewas 1990s isolated [19 ,in22 ],the but 1990s its structure[19,22], but is stillits structure unknown. is still It is unknown 1.6-fold. less It is toxic1.6-fold than less MTX1 toxic bythan i.p. MTX1 injection by i.p. [23 injection]. The structure[23]. The of structure MTX3 was of MTX3 recently was elucidated recently andelucidated corresponds and c toorresponds 44-methyl to gambierone 44-methyl withgam- abierone molecular with weight a molecular of 1/3 MTX1weight and of 1/3 has MTX1 very lowand CTX-likehas very activity,low CTX possibly-like activity, related possibly to the sulfaterelated group to the in sulfate its structure group (Figure in its structure1)[ 24,25]. (Figure Therefore, 1) [24,25]. the compound Therefore, previously the compound called MTX3previously is referred called to MTX3 as 44-methyl is referred gambierone to as 44-methyl rather thangambierone MTX3. However,rather than recent MTX3. studies How- suggestever, recent that MTX3studies is suggest not 44-methyl that MTX3 gambierone is not 44 due-methyl to the gambierone low toxicity due and to inconsistent the low tox- signsicity and reported inconsistent for 44-methyl signs reported gambierone for 44 compared-methyl gambierone with MTX3 [compared26]. Further with research MTX3 will[26]. beFurther needed research to confirm will if be these needed compounds, to confirm which if thes mighte compounds, not be biologically which might equivalent, not be arebio- thelogical samely molecule.equivalent, Desulfo-MTX1 are the same and molecule. didehydro-demethyl-desulfo-MTX1 Desulfo-MTX1 and didehydro were-demethyl partially- elucidated,desulfo-MTX1 being were isolated partially from G.elucidated, belizeanus beingstrain isolated CCMP 399 from and G.Gambierdiscus belizeanus strainribotype-2 CCMP strain399 and CCMP Gambierdiscus 1655, respectively, ribotype from-2 strain the CCMP Caribbean 1655 Sea,, respectively, and their biological from the Caribbean activity is stillSea, unknownand their [biological21]. activity is still unknown [21]. FigureFigure 1. 1.Structures Structures of of MTX1 MTX1 and and 44-methyl-gambierone 44-methyl-gambierone (MTX3). (MTX3). SurveillanceSurveillance programs programs are are being being globally globally implemented implemented to to evaluate evaluate the the presence presence and and spreadspread of of
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