Abstract
Some benthic Prorocentrum can produce okadaic acid (OA) and dinophysistoxins (DTXs) that cause diarrheic shellfish poisoning (DSP) in humans. The diversity and toxin profiles (OA and DTXs) of benthic Prorocentrum were investigated in the Xisha Islands, South China Sea. The benthic Prorocentrum was identified by both morphological features and molecular phylogenies. Morphologies were examined by light, fluorescence, and scanning electron microscopy, and phylogenetic analyses were based on partial large subunit (LSU) rDNA and ITS1-5.8S-ITS2 (ITS) region. Seven Prorocentrum species including P. borbonicum, P. caipirignum, P. concavum, P. elegans, P. cf. emarginatum, P. lima complex, and P. rhathymum were identified in Xisha Islands. Among them, P. borbonicum and P. elegans were recorded in Chinese waters for the first time. OA and DTXs contents of seven benthic Prorocentrum species were evaluated based on liquid chromatography-tandem mass spectrometry (LC-MS/MS). All Xisha Islands strains of P. lima complex produced OA at contents ranging from 1 663 to 3 816 fg/cell. P. caipirignum also generated OA at 407 fg/cell, but other five species had no detectable toxins. Besides, interestingly, two strains of P. lima complex produced DTX-1 only (74 and 183 fg/cell) and another two strains generated an isomer of OA and DTX-2. Our findings provided insight into the biodiversity of benthic Prorocentrum in the Xisha Islands and pointed out the potential risk of DSP in this area.
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Data Availability Statement
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Accoroni S, Totti C. 2016. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: a review. Advances in Oceanography and Limnology, 7(1): 1–15, https://doi.org/10.4081/aiol.2016.5591.
Aligizaki K, Nikolaidis G, Katikou P, Baxevanis A D, Abatzopoulos T J. 2009. Potentially toxic epiphytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae, 8(2): 299–311, https://doi.org/10.1016/j.hal.2008.07.002.
Amar M, Aráoz R, Iorga B I, Yasumoto T, Servent D, Molgó J. 2018. Prorocentrolide-A from cultured Prorocentrum lima dinoflagellates collected in Japan blocks sub-types of nicotinic acetylcholine receptors. Toxins, 10(3): 97, https://doi.org/10.3390/toxins10030097.
An T Y, Winshell J, Scorzetti G, Fell J W, Rein K S. 2010. Identification of okadaic acid production in the marine dinoflagellate Prorocentrum rhathymum from Florida Bay. Toxicon, 55(2–3): 653–657, https://doi.org/10.1016/j.toxicon.2009.08.018.
Aquino-Cruz A, Purdie D A, Morris S. 2018. Effect of increasing sea water temperature on the growth and toxin production of the benthic dinoflagellate Prorocentrum lima. Hydrobiologia, 813(1): 103–122, https://doi.org/10.1007/s10750-018-3512-4.
Berdalet E, Bravo I, Evans J, Fraga S, Kibler S, Kudela R, Larsen J, Litaker W, Penna A, Tester P A, Vila M, Zingone A. 2012. Global Ecology and Oceanography of Harmful Algal Blooms, GEOHAB Core Research Project: HABs in Benthic Systems. GEOHAB, Paris.
Berdalet E, Tester P A, Chinain M, Fraga S, Lemée R, Litaker W, Penna A, Usup G, Vila M, Zingone A. 2017. Harmful algal blooms in benthic systems: recent progress and future research. Oceanography, 30(1): 36–45, https://doi.org/10.5670/oceanog.2017.108.
Boisnoir A, Pascal P Y, Cordonnier S, Lemée R. 2019. Spatiotemporal dynamics and biotic substrate preferences of benthic dinoflagellates in the Lesser Antilles, Caribbean sea. Harmful Algae, 81: 18–29, https://doi.org/10.1016/j.hal.2018.11.012.
Bouaïcha N, Chézeau A, Turquet J, Quod J P, Puiseux-Dao S. 2001. Morphological and toxicological variability of Prorocentrum lima clones isolated from four locations in the south-west Indian Ocean. Toxicon, 39(8): 1195–1202, https://doi.org/10.1016/S0041-0101(00)00258-0.
Caillaud A, de la Iglesia P, Campàs M, Elandaloussi L, Fernández M, Mohammad-Noor N, Andree K, Diogène J. 2010. Evidence of okadaic acid production in a cultured strain of the marine dinoflagellate Prorocentrum rhathymum from Malaysia. Toxicon, 55(2–3): 633–637, https://doi.org/10.1016/toxicon.2009.07.016.
Chomérat N, Bilien G, Zentz F. 2019. A taxonomical study of benthic Prorocentrum species (Prorocentrales, Dinophyceae) from Anse Dufour (Martinique Island, eastern Caribbean Sea). Marine Biodiversity, 49(3): 1299–1319, https://doi.org/10.1007/s12526-018-0913-6.
David H, Laza-Martínez A, García-Etxebarria K, Riobó P, Orive E. 2014. Characterization of Prorocentrum elegans and Prorocentrum levis (Dinophyceae) from the southeastern Bay of Biscay by morphology and molecular phylogeny. Journal of Phycology, 50(4): 718–726, https://doi.org/10.1111/jpy.12200.
Dickey R W, Bobzin S C, Faulkner D J, Bencsath F A, Andrzejewski D. 1990. Identification of okadaic acid from a Caribbean dinoflagellate, Prorocentrum concavum. Toxicon, 28(4): 371–377, https://doi.org/10.1016/0041-0101(90)90074-H.
Ehrenberg C G. 1834. Dritter Beitrag zur Erkenntnis grosser organisationen in der Richtung des kleinsten raumes. Abhandlungen der Königlichen. Akademie der Wissenschaften, Berlin, Germany, 1833: 145–336.
Escoffier N, Gaudin J, Mezhoud K, Huet H, Chateau-Joubert S, Turquet J, Crespeau F, Edery M. 2007. Toxicity to medaka fish embryo development of okadaic acid and crude extracts of Prorocentrum dinoflagellates. Toxicon, 49(8): 1182–1192, https://doi.org/10.1016/j.toxicon.2007.02.008.
Faust M A. 1993. Prorocentrum belizeanum, Prorocentrum elegans, and Prorocentrum caribbaeum, three new benthic species (Dinophyceae) from a mangrove island, Twin Cays, Belize. Journal of Phycology, 29(1): 100–107, https://doi.org/10.1111/j.1529-8817.1993.tb00287.x.
Fensome R, Taylor F, Norris G, Sarjeant W A S., 1993. A Classification of Living and Fossil Dinoflagellates: Geological Survey of Canada Contribution, Micropaleontology. American Museum of Natural History, Salem.
Foden J, Purdie D A, Morris S, Nascimento S. 2005. Epiphytic abundance and toxicity of Prorocentrum lima populations in the Fleet Lagoon, UK. Harmful Algae, 4(6): 1063–1074, https://doi.org/10.1016/j.hal.2005.03.004.
Fukuyo Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Nippon Suisan Gakkaishi, 47(8): 967–978, https://doi.org/10.2331/suisan.47.967.
Gómez F, Qiu D J, Lin S J. 2017. The synonymy of the toxic dinoflagellates Prorocentrum mexicanum and P. rhathymum and the description of P. steidingerae sp. nov. (Prorocentrales, Dinophyceae). Journal of Eukaryotic Microbiology, 64(5): 668–677, https://doi.org/10.1111/jeu.12403.
Goris J, Hermann J, Hendrix P, Ozon R, Merlevede W. 1989. Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. FEBS Letters, 245(1–2): 91–94, https://doi.org/10.1016/0014-5793(89)80198-X.
Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3): 234–236, https://doi.org/10.2216/i0031-8884-32-3-234.1.
Heredia-Tapia A, Arredondo-Vega B O, Nuñez-Vázquez E J, Yasumoto T, Yasuda M, Ochoa J L. 2002. Isolation of Prorocentrum lima (Syn. Exuviaella lima) and diarrhetic shellfish poisoning (DSP) risk assessment in the Gulf of California, Mexico. Toxicon, 40(8): 1121–1127, https://doi.org/10.1016/S0041-0101(02)00111-3.
Hoppenrath M, Chomérat N, Horiguchi T, Schweikert M, Nagahama Y, Murray S. 2013. Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae)—a proposal and review. Harmful Algae, 27: 1–28, https://doi.org/10.1016/j.hal.2013.03.006.
Juranovic L R, Park D L, Fremy J M, Nielsen C A, Ah S S, Ayala C E. 1997. Isolation and separation of toxins produced by Gambierdiscus toxicus and Prorocentrum concavum. Journal of Aquatic Food Product Technology, 6(4): 5–25, https://doi.org/10.1300/J030v06n04_02.
Lim Z F, Luo Z H, Lee L K, Hii K S, Teng S T, Chan L L, Chomérat N, Krock B, Gu H F, Lim P T, Leaw C P. 2019. Taxonomy and toxicity of Prorocentrum from Perhentian Islands (Malaysia), with a description of a non-toxigenic species Prorocentrum malayense sp. nov. (Dinophyceae). Harmful Algae, 83: 95–108, https://doi.org/10.1016/j.hal.2019.01.007.
Luo Z H, Zhang H, Krock B, Lu S H, Yang W D, Gu H F. 2017. Morphology, molecular phylogeny and okadaic acid production of epibenthic Prorocentrum (Dinophyceae) species from the northern South China Sea. Algal Research, 22: 14–30, https://doi.org/10.1016/j.algal.2016.11.020.
Marasigan AN, Sato S, Fukuyo Y, Kodama M. 2001. Accumulation of a high level of diarrhetic shellfish toxins in the green mussel Perna viridis during a bloom of Dinophysis caudata and Dinophysis miles in Sapian Bay, Panay Island, the Philippines. Fisheries Science, 67(5): 994–996, https://doi.org/10.1046/j.1444-2906.2001.00353.x.
Mohammad-Noor N, Moestrup Ø, Daugbjerg N. 2007. Light, electron microscopy and DNA sequences of the dinoflagellate Prorocentrum concavum (syn. P. arabianum) with special emphasis on the periflagellar area. Phycologia, 46(5): 549–564.
Morton S L. 1998. Morphology and toxicology of Prorocentrum faustiae sp. nov., a toxic species of non-planktonic dinoflagellate from Heron Island, Australia. Botanica Marina, 41(1–6): 565–569, https://doi.org/10.1515/botm.1998.41.1-6.565.
Murray S, Ip C L C, Moore R, Nagahama Y, Fukuyo Y. 2009. Are prorocentroid dinoflagellates monophyletic? A study of 25 species based on nuclear and mitochondrial genes. Protist, 160(2): 245–264, https://doi.org/10.1016/j.protis.2008.12.004.
Nascimento S M, Mendes M C Q, Menezes M, Rodríguez F, Alves-De-souza C, Branco S, Riobó P, Franco J, Nunes J M C, Huk M, Morris S, Fraga S. 2017. Morphology and phylogeny of Prorocentrum caipirignum sp. nov. (Dinophyceae), a new tropical toxic benthic dinoflagellate. Harmful Algae, 70: 73–89, https://doi.org/10.1016/j.hal.2017.11.001.
Nishimura T, Uchida H, Noguchi R, Oikawa H, Suzuki T, Funaki H, Ihara C, Hagino K, Arimitsu S, Tanii Y, Abe S, Hashimoto K, Mimura K, Tanaka K, Yanagida I, Adachi M. 2020a. Abundance of the benthic dinoflagellate Prorocentrum and the diversity, distribution, and diarrhetic shellfish toxin production of Prorocentrum lima complex and P. caipirignum in Japan. Harmful Algae, 96: 101687, https://doi.org/10.1016/j.hal.2019.101687.
Nishimura T, Uchida H, Suzuki T, Tawong W, Abe S, Arimitsu S, Adachi M. 2020b. First report on okadaic acid production of a benthic dinoflagellate Prorocentrum cf. fukuyoi from Japan. Phycological Research, 68(1): 30–40, https://doi.org/10.1111/pre.12401.
Pan L, Chen J H, Shen H H, He X P, Li G J, Song X C, Zhou D S, Sun C J. 2017. Profiling of extracellular toxins associated with diarrhetic shellfish poison in Prorocentrum lima culture medium by high-performance liquid chromatography coupled with mass spectrometry. Toxins, 9(10): 308, https://doi.org/10.3390/toxins9100308.
Pin L C, Teen L P, Ahmad A, Usup G. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Marine Biotechnology, 3(3): 246–255, https://doi.org/10.1007/s101260000073.
Rodríguez F, Riobó P, Crespín G D, Daranas A H, De Vera C R, Norte M, Fernández J J, Fraga S. 2018. The toxic benthic dinoflagellate Prorocentrum maculosum Faust is a synonym of Prorocentrum hoffmannianum Faust. Harmful Algae, 78: 1–8, https://doi.org/10.1016/j.hal.2018.06.009.
Scholin C A, Herzog M, Sogin M, Anderson D M. 1994. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. sequence analysis of a fragment of the LSU rRNA gene. Journal of Phycology, 30(6): 999–1011, https://doi.org/10.1111/j.0022-3646.1994.00999.x.
Ten-Hage L C, Delaunay N, Pichon V, Couté A, Puiseux-Dao S, Turquet J. 2000b. Okadaic acid production from the marine benthic dinoflagellate Prorocentrum arenarium Faust (Dinophyceae) isolated from Europa Island coral reef ecosystem (SW Indian Ocean). Toxicon, 38(8): 1043–1054, https://doi.org/10.1016/S0041-0101(99)00216-0.
Ten-Hage L, Robillot C, Turquet J, Le Gall F, Le Caer J P, Bultel V, Guyot M, Molgó J. 2002. Effects of toxic extracts and purified borbotoxins from Prorocentrum borbonicum (Dinophyceae) on vertebrate neuromuscular junctions. Toxicon, 40(2): 137–148, https://doi.org/10.1016/S0041-0101(01)00200-8.
Ten-Hage L, Turquet J, Quod J P, Puiseux-Dao S, Coute A. 2000a. Prorocentrum borbonicum sp. nov. (Dinophyceae), a new toxic benthic dinoflagellate from the southwestern Indian Ocean. Phycologia, 39(4): 296–301, https://doi.org/10.2216/i0031-8884-39-4-296.1.
Toyofuku H. 2006. Joint FAO/WHO/IOC activities to provide scientific advice on marine biotoxins (research report). Marine Pollution Bulletin, 52(12): 1735–1745, https://doi.org/10.1016/j.marpolbul.2006.07.007.
Vale P, Veloso V, Amorim A. 2009. Toxin composition of a Prorocentrum lima strain isolated from the Portuguese coast. Toxicon, 54(2): 145–152, https://doi.org/10.1016/j.toxicon.2009.03.026.
Vila M, Garcés E, Masó M. 2001. Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquatic Microbial Ecology, 26(1): 51–60, https://doi.org/10.3354/ame026051.
Yasumoto T, Seino N, Murakami Y, Murata M. 1987. Toxins produced by benthic dinoflagellates. The Biological Bulletin, 172(1): 128–131, https://doi.org/10.2307/1541612.
Zhang H, Li Y, Cen J Y, Wang H L, Cui L, Dong Y L, Lu S H. 2015. Morphotypes of Prorocentrum lima (Dinophyceae) from Hainan Island, South China Sea: morphological and molecular characterization. Pycologia, 54(5): 503–516, https://doi.org/10.2216/15-8.1.
Zhou J, Fritz L. 1993. Ultrastructure of two toxic marine dinoflagellates, Prorocentrum lima and Prorocentrum maculosum. Phycologia, 32(6): 444–450, https://doi.org/10.2216/i0031-8884-32-6-444.1.
Zou J, Li Q, Lu S H, Dong Y L, Chen H, Zheng C Z, Cui L. 2020. The first benthic harmful dinoflagellate bloom in China: Morphology and toxicology of Prorocentrum concavum. Marine Pollution Bulletin, 158: 111313, https://doi.org/10.1016/j.marpolbul.2020.111313.
Acknowledgment
We sincerely appreciate the three anonymous reviewers’ comments and suggestions, which are helpful for the manuscript. Prof. Yubo LIANG from the National Marine Environmental Monitoring Center is deeply appreciated for providing data about toxins. We also thank Prof. Aifeng LI for providing valuable suggestions for the paper revision.
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Supported by the National Natural Science Foundation of China (Nos. 41876173, 41606176, 41576162, 41606175) and the Special Foundation for National Science and Technology Basic Research Program of China (Nos. 2018FY100200, 2018FY100100)
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Zou, J., Li, Q., Liu, H. et al. Taxonomy and toxin profile of harmful benthic Prorocentrum (Dinophyceae) species from the Xisha Islands, South China Sea. J. Ocean. Limnol. 40, 1171–1190 (2022). https://doi.org/10.1007/s00343-021-1045-6
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DOI: https://doi.org/10.1007/s00343-021-1045-6