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Toxin Profiles of Okadaic Acid Analogues and Other Lipophilic

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Toxin Profiles of Okadaic Acid Analogues and Other Lipophilic toxins Article Toxin Profiles of Okadaic Acid Analogues and Other Lipophilic Toxins in Dinophysis from Japanese Coastal Waters Hajime Uchida 1, Ryuichi Watanabe 1, Ryoji Matsushima 1, Hiroshi Oikawa 1, Satoshi Nagai 1, Takashi Kamiyama 2, Katsuhisa Baba 3, Akira Miyazono 4, Yuki Kosaka 5, Shinnosuke Kaga 6, Yukihiko Matsuyama 7 and Toshiyuki Suzuki 1,* 1 National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa-ku, Yokohama, Kanagawa 236-8648, Japan; [email protected] (H.U.); [email protected] (R.W.); [email protected] (R.M.); [email protected] (H.O.); [email protected] (S.N.) 2 National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and Education Agency, 2-17-5, Maruishi, Hatsukaichi, Hiroshima 739-0452, Japan; [email protected] 3 Central Fisheries Research Institute, Fisheries Research Department, Hokkaido Research Organization, 238, Hamanakacho, Yoichi-cho, Yoichi-gun, Hokkaido 046-8555, Japan; [email protected] 4 Kushiro Fisheries Research Institute, Fisheries Research Department, Hokkaido Research Organization, 4-25, Nakahamacho, Kushiro-city, Hokkaido 085-0027, Japan; [email protected] 5 Aomori Prefectural Industrial Technology Research Center, Fisheries Research Institute, Hiranai, Higashitsugarugun, Aomori 039-3381, Japan; [email protected] 6 Iwate Fisheries Technology Center, 3-75-3 Hirata, Kamaishi, Iwate 026-0001, Japan; [email protected] 7 Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, 1551-8, Taira-machi, Nagasaki-shi, Nagasaki 851-2213, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-45-788-7662; Fax: +81-45-788-5001 Received: 23 September 2018; Accepted: 4 November 2018; Published: 6 November 2018 Abstract: The identification and quantification of okadaic acid (OA)/dinophysistoxin (DTX) analogues and pectenotoxins (PTXs) in Dinophysis samples collected from coastal locations around Japan were evaluated by liquid chromatography mass spectrometry. The species identified and analyzed included Dinophysis fortii, D. acuminata, D. mitra (Phalacroma mitra), D. norvegica, D. infundibulus, D. tripos, D. caudata, D. rotundata (Phalacroma rotundatum), and D. rudgei. The dominant toxin found in D. acuminata was PTX2 although some samples contained DTX1 as a minor toxin. D. acuminata specimens isolated from the southwestern regions (Takada and Hiroshima) showed characteristic toxin profiles, with only OA detected in samples collected from Takada. In contrast, both OA and DTX1, in addition to a larger proportion of PTX2, were detected in D. acuminata from Hiroshima. D. fortii showed a toxin profile dominated by PTX2 although this species had higher levels of DTX1 than D. acuminata. OA was detected as a minor toxin in some D. fortii samples collected from Yakumo, Noheji, and Hakata. PTX2 was also the dominant toxin found among other Dinophysis species analyzed, such as D. norvegica, D. tripos, and D. caudata, although some pooled picked cells of these species contained trace levels of OA or DTX1. The results obtained in this study re-confirm that cellular toxin content and profiles are different even among strains of the same species. Keywords: Dinophysis; diarrhetic shellfish poisoning; marine toxins; pectenotoxin; okadaic acid; dinophysistoxin Key Contribution: Pooled picked cells of Dinophysis species collected from locations around Japan were analyzed by liquid chromatography mass spectrometry to determine their toxin content and relative toxin profiles. Toxins 2018, 10, 457; doi:10.3390/toxins10110457 www.mdpi.com/journal/toxins Toxins 2018, 10, x FOR PEER REVIEW 2 of 14 Toxins 2018, 10, 457 2 of 14 1. Introduction 1. Introduction The diarrhetic shellfish toxins (DSTs), okadaic acid (OA) and dinophysistoxins (DTXs), as well as pectenotoxinsThe diarrhetic (PTXs) shellfish (Figure toxins 1) [1], (DSTs), are produced okadaic acid by (OA)planktonic and dinophysistoxins species of the genus, (DTXs), Dinophysis as well andas pectenotoxins benthic species (PTXs) of Prorocentrum (Figure1)[ 1[2].], are Bivalves produced become by planktonic contaminat speciesed with of these the genus, marineDinophysis toxins by feedingand benthic on toxic species Dinophysis of Prorocentrum species. The[2]. regulation Bivalves become of DSTs contaminated recommended with by Codex these marineAlimentarius toxins [3] by isfeeding 160 ng on OA toxic equivalent/gDinophysis inspecies. the edible The part regulation of bivalves. of DSTs The recommended regulation in bythe Codex European Alimentarius Union (EU) [3] is 160a total ng OAof 160 equivalent/g ng OA/DTX in and the ediblePTXs/g part in the of bivalves. edible part The of regulation bivalves [4]. in the The European cellular Uniontoxin content (EU) is anda total profiles of 160 of ng several OA/DTX Dinophysis and PTXs/g species inhave the been edible reported part of by bivalves analyzing [4]. field The cellularmultispecific toxin samples content obtainedand profiles by ofplankton several netDinophysis hauls, orspecies monospecific have been cultures. reported [5–18]. by analyzing However, field it remains multispecific important samples to updateobtained toxin by planktoncontent and net hauls,profile orinformation monospecific of Dinophysis cultures [5 –species18]. However, to improve it remains the prediction important of bivalveto update contamination. toxin content The and cellular profile toxin information content ofandDinophysis profiles ofspecies Dinophysis to improve species theof pooled prediction picked of cellsbivalve reported contamination. in previous The studies cellular was toxin revised content (Table and 1) profiles [19–35]. of AnalysisDinophysis of individuallyspecies of pooled picked picked cells wascells historically reported in the previous only unambiguous studies was revised way to (Table ascribe1)[ a19 toxin–35]. profile Analysis and of content individually information picked cellsto a wasDinophysis historically species, the until only unambiguous2006, when cultures way to of ascribe D. acuminata a toxin profilebecame and available content [36]. information Because tothe a Dinophysiscellular toxinspecies, content until and 2006, profiles when are cultures different of D. even acuminata amongbecame samples available of the same [36]. Becausespecies [36,37], the cellular it is necessarytoxin content to clarify and profiles cellular are to differentxin contents even amongand profiles samples of ofDinophysis the same spp. species present [36,37 in], iteach is necessary bivalve monitoringto clarify cellular area. toxin contents and profiles of Dinophysis spp. present in each bivalve monitoring area. Figure 1. ChemicalChemical structure structure of okadaic okadaic acid acid (OA) (OA) an andd dinophysistoxin dinophysistoxin (DTX) (DTX) and and pectenotoxin pectenotoxin (PTX) (PTX) analogues found in Dinophysis species. ( a) OA and DTX analogues. ( b) PTX2 and PTX11. Historically, DST contamination of bivalves, and associated human poisoning cases, were restricted in in the the northeastern northeastern regions regions of of Japan Japan (T (Tohokuohoku and and Hokkaido Hokkaido area). area). Therefore, Therefore, data data on the on toxinthe toxin content content and and profiles profiles of ofDinophysisDinophysis fromfrom these these regions regions is is essential essential for for predicting predicting bivalve contamination. Although Dinophysis occurs in the southwestern part partss of Japan, no toxin information has beenbeen reportedreported for forDinophysis Dinophysisspecies species found found there. there. It is interestingIt is interesting that DST that positive DST positive cases in bivalvescases in bivalvesobtained withobtained the previous with the DST previous official testing DST methodofficial (mousetesting bioassay)method in(mouse the southwestern bioassay) partsin the of Japansouthwestern have hardly parts been of Japan reported. have hardly been reported. Between 2006 and 2014, pooled picked cells of many Dinophysis species were generated from seawater samples samples taken taken from from many many locations locations around around the the Japanese Japanese coastline. coastline. DSTs DSTsand PTXs and PTXswere wereextracted extracted using usinga solid a phase solid extraction phase extraction method method [6,19,23], [6 and,19,23 the], andextracts the kept extracts frozen kept until frozen analysis. until Inanalysis. this study, In this the study, presence the presenceof DSTs ofand DSTs PTXs and in PTXsthese insamples these sampleswas determined was determined by liquid by chromatographyliquid chromatography triple triplequadrupole quadrupole tandem tandem mass mass spectrometry spectrometry (LC/MS/MS) (LC/MS/MS) [23] [23 ]and and liquid chromatography quadrupole mass spectrometry (LC/MS)(LC/MS) [38]. [38]. Toxins 2018, 10, 457 3 of 14 Table 1. Reported toxin content and profiles in pooled picked cell isolates of Dinophysis field specimens. pg/cell Species Location Analysis Method Reference OA DTX1 DTX2 PTX2 Dinophysis acuminata 1.6 - - - Le Havre, France HPLC-FLD [19] Trace - - - Tokyo Bay, Japan HPLC-FLD [19] 9.1 - - - Gullmar, Sweden HPLC-FLD [20] 9.9–21.7 - - - Galicia, Spain HPLC-FLD [21] - - - 180.0 Bahia Inglesa, Chile LC/MS/MS [22] - 0.3–0.7 - 10.7–22.4 Abashiri, Japan LC/MS/MS [23] - ND–0.7 - 25.9–50.2 Yakumo, Japan LC/MS/MS [23] ND–0.8 - - 0.9–8.7 Flødevigen Bay, Noway LC/MS/MS [24] 3.7 - - - Bueu, Spain LC/MS/MS [25] Dinophysis fortii - 13.0–191.5
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