Abstract
About 30 benthic Prorocentrum species have been described, some of which producing okadaic acid and derivatives involved in diarrhetic shellfish poisoning. The western Caribbean has been extensively studied for benthic dinoflagellates associated with ciguatera, and fifteen Prorocentrum species were described from mangroves and coral reefs of Belize. In contrast, no study reported the diversity of this genus in the Eastern Caribbean, especially in the Lesser Antilles. This study adds to the biodiversity knowledge in Martinique Island by investigating one site of the Caribbean coast from 2010 to 2017. Sediment samples were collected each year in March and studied taxonomically. Identification was realized morphologically by scanning electron microscopy, while the partial large subunit (LSU) ribosomal DNA was sequenced for 42 isolated specimens (single-cells) and one strain in culture. A molecular phylogenetic analysis revealed 11 OTUs from Martinique, identified morphologically as P. concavum, P. cf. foraminosum, P. cf. tropicale, P. lima, P. hoffmannianum, P. cf. norrisianum, P. glenanicum, P. panamense, P. cf. sculptile, P. cf. fukuyoi, and P. rhathymum. Two morphospecies were also identified (P. cf. maculosum and P. cf. ruetzlerianum) but with no sequence obtained. Some species like P. cf. tropicale and P. cf. norrisinamum are sequenced for the first time. Our analysis reveals probable former misidentifications of P. cf. foraminosum and P. cf. sculptile since the sequences from Martinique form new clades and their geographical origin are closer from the type locality than any other previous studies. Further studies and sequences from the type localities are yet required to assess identifications.
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Aligizaki K, Nikolaidis G, Katikou P, Baxevanis AD, Abatzopoulos TJ (2009) Potentially toxic epiphytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae 8:299–311
Besada EG, Loeblich LA, Loeblich ARIII (1982) Observations on tropical, benthic dinoflagellates from ciguatera-endemic areas: Coolia, Gambierdiscus and Ostreopsis. Bull Mar Sci 32:723–735
Boisnoir A, Pascal P-Y, Cordonnier S, Lemée R (2018) Depth distribution of benthic dinoflagellates in the Caribbean Sea. J Sea Res 135:74–83. https://doi.org/10.1016/j.seares.2018.02.001
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 39:1195–1202
Chomérat N, Bilien G (2014) Madanidinium loirii gen. et sp. nov. (Dinophyceae), a new marine benthic dinoflagellate from Martinique Island, Eastern Caribbean. Eur J Phycol 49:165–178
Chomérat N, Couté A (2008) Protoperidinium bolmonense sp. nov. (Peridiniales, Dinophyceae), a small dinoflagellate from a brackish hypereutrophic lagoon (South of France). Phycologia 47:392–403
Chomérat N, Saburova M, Bilien G, Al-Yamani F (2012) Prorocentrum bimaculatum sp. nov. (Dinophyceae, Prorocentrales), a new benthic dinoflagellate species from Kuwait (Arabian gulf). J Phycol 48:211–221
Chomérat N, Zentz F, Boulben S, Bilien G, van Wormhoudt A, Nézan E (2011) Prorocentrum glenanicum sp. nov. and P. pseudopanamense sp. nov. (Prorocentrales, Dinophyceae), two new benthic dinoflagellate species from South Brittany (northwestern France). Phycologia 50:202–214
Ehrenberg CG (1834) Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin 1833:145–336
Ehrenberg CG (1860) Über das Leuchten und über neue mikroskopische Leuchtthiere des Mittelmeeres. Königliche Preussische Akademie der Wissenschaften zu Berlin, Verhandlungen, Monatsberichte 1859:791–793
Faust MA (1990a) Morphologic details of six benthic species of Prorocentrum (Pyrrophyta) from a mangrove island, Twin Cays, Belize, including two new species. J Phycol 26:548–558
Faust MA (1990b) Cysts of Prorocentrum marinum (Dinophyceae) in floating detritus at Twin Cays, Belize mangrove habitats. In: Granéli E, Sundstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier Science Publishing, New-York, pp 138–143
Faust MA (1991) Morphology of ciguatera-causing Prorocentrum lima (Pyrrophyta) from widely differing sites. J Phycol 27:642–648
Faust MA (1993a) Prorocentrum belizeanum, Prorocentrum elegans, and Prorocentrum caribbaeum, three new benthic species (Dinophyceae), from a mangrove island, Twin Cays, Belize. J Phycol 29:100–107
Faust MA (1993b) Three new benthic species of Prorocentrum (Dinophyceae) from Twin Cays, Belize: P. maculosum sp. nov., P. foraminosum sp. nov. and P. formosum sp. nov. Phycologia 32:410–418
Faust MA (1994) Three new benthic species of Prorocentrum (Dinophyceae) from Carrie Bow Cay, Belize: P. sabulosum sp. nov., P. sculptile sp. nov. and P. arenarium sp. nov. J Phycol 30:755–763
Faust MA (1995) Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J Phycol 31:996–1003
Faust MA (1996) Dinoflagellates in a mangrove ecosystem, Twin Cays, Belize. Nova Hedwig 112:447–460
Faust MA (1997) Three new benthic species of Prorocentrum (Dinophyceae) from Belize: P. norrisianum sp. nov., P. tropicalis sp. nov., and P. reticulatum sp. nov. J Phycol 33:851–858
Faust MA (1999) Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribbeanus sp. nov. Phycologia 38:92–99
Faust MA (2000) Dinoflagellate associations in a coral reef-mangrove ecosystem: pelican and associated cays, Belize. Atoll Res Bull 473:133–149
Faust MA (2009) Ciguatera-causing dinoflagellates in a coral-reef-mangrove ecosystem, Belize. Atoll Res Bull (569):1–30. https://doi.org/10.5479/si.00775630.569.1
Faust MA, Gulledge RA (2002) Identifying harmful marine dinoflagellates. Smithson Inst Contrib U S Natl Herb 42:1–144
Faust MA, Larsen J, Moestrup Ø (1999) Leaflet no. 184—potentially toxic phytoplankton. 3. Genus Prorocentrum. In: Lindley JA (ed) ICES identification leaflets for plankton. International Council for the Exploration of the Sea, Copenhagen, pp 1–24
Faust MA, Morton SL (1995) Morphology and ecology of the marine dinoflagellate Ostreopsis labens sp. nov. (Dinophyceae). J Phycol 31:456–463
Faust MA, Vandersea MW, Kibler SR, Tester PA, Litaker RW (2008) Prorocentrum levis, a new benthic species (Dinophyceae) from a mangrove island, Twin Cays, Belize. J Phycol 44:232–240
Fukuyo Y (1981) Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull Jpn Soc Sci Fish 47:967–978
Grzebyk D, Sako Y, Berland B (1998) Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons, and description of Prorocentrum panamensis, sp. nov. J Phycol 34:1055–1068
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication. http://www.algaebase.org. Accessed 28 Mar 2018
Herrera-Sepúlveda A, Medlin LK, Murugan G, Sierra-Beltrán AP, Cruz-Villacorta AA, Hernández-Saavedra NY, Müller K (2015) Are Prorocentrum hoffmannianum and Prorocentrum belizeanum (Dinophyceae, Prorocentrales), the same species? An integration of morphological and molecular data. J Phycol 51:173–188. https://doi.org/10.1111/jpy.12265
Hoppenrath M (2017) Dinoflagellate taxonomy—a review and proposal of a revised classification. Mar Biodivers 47:381–403. https://doi.org/10.1007/s12526-016-0471-8
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
Hoppenrath M, Murray S, Chomérat N, Horiguchi T (2014) Marine benthic dinoflagellates - unveiling their worldwide biodiversity (Kleine Senckenberg-Reihe 54). E. Schweizerbart’sche Verlagbuchhandlung
Hoppenrath M, Saldarriaga JF, Schweikert M, Elbrächter M, Taylor FJR (2004) Description of Thecadinium mucosum sp. nov. (Dinophyceae), a new sand-dwelling marine dinoflagellate, and an emended description of Thecadinium inclinatum Balech. J Phycol 40:946–961
Kameneva PA, Efimova KV, Rybin VG, Orlova TY (2015) Detection of Dinophysistoxin-1 in clonal culture of marine dinoflagellate Prorocentrum foraminosum (Faust M.A., 1993) from the Sea of Japan. Toxins Basel 7:3947–3959. https://doi.org/10.3390/toxins7103947
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6(29)
Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Lassus P, Chomérat N, Hess P, Nézan E (2016) Toxic and harmful microalgae of the world ocean. UNESCO, Denmark
Laza-Martínez A, Orive E, Irati M (2011) Morphological and genetic characterization of benthic dinoflagellates of the genera Coolia, Ostreopsis and Prorocentrum from south-eastern Bay of Biscay. Eur J Phycol 46:45–65
Litaker RW, Vandersea MW, Faust MA, Kibler SR, Nau AW, Holland WC, Chinain M, Holmes MJ, Tester PA (2010) Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 56:711–730. https://doi.org/10.1016/j.toxicon.2010.05.017
Loeblich AR, Sherley JL, Schmidt RJ (1979) The correct position of flagellar insertion in Prorocentrum and description of Prorocentrum rhathymum sp. nov. (Pyrrhophyta). J Plankton Res 1:113–120. https://doi.org/10.1093/plankt/1.2.113
Luo Z, Zhang H, Krock B, Lu S, Yang W, Gu H (2017) Morphology, molecular phylogeny and okadaic acid production of epibenthic Prorocentrum (Dinophyceae) species from the northern South China Sea. Algal Res 22:14–30. https://doi.org/10.1016/j.algal.2016.11.020
Mertens KN, Gu H, Pospelova V, Chomérat N, Nézan E, Gurdebeke P, Bogus K, Vrielinck H, Rumèbe M, Méteigner C (2017) First recod of resting cysts of the benthic dinoflagellate Prorocentrum leve in a natural reservoir in Gujan-Mestras, Gironde, France. J Phycol 53:1193–1205. https://doi.org/10.1111/jpy.12582
Mohammad-Noor N, Daugbjerg N, Moestrup Ø, Anton A (2007a) Marine epibenthic dinoflagellates from Malaysia—a study of live cultures and preserved samples based on light and scanning electron microscopy. Nord J Bot 24:629–690
Mohammad-Noor N, Moestrup Ø, Daugbjerg N (2007b) Light, electron microscopy and DNA sequences of the dinoflagellate Prorocentrum concavum (syn. P. arabianum) with special emphasis on the periflagellar area. Phycologia 46:549–564
Morton SL (1998) Morphology and toxicology of Prorocentrum faustiae sp. nov., a toxic species of non planktonic dinoflagellate from Heron Island, Australia. Bot Mar 41:565–569
Morton SL, Faust MA, Fairey EA, Moeller PDR (2002) Morphology and toxicology of Prorocentrum arabianum sp. nov., (dinophyceae) a toxic planktonic dinoflagellate from the Gulf of Oman, Arabian Sea. Harmful Algae 8:393–400
Murray S, Ip CLC, Moore R, Nagahama Y, Fukuyo Y (2009) Are prorocentroid dinoflagellates monophyletic? A study of 25 species based on nuclear and mitochondrial genes. Protist 160:245–264
Murray S, Nagahama Y, Fukuyo Y (2007) Phylogenetic study of benthic, spine-bearing prorocentroids, including Prorocentrum fukuyoi sp. nov. Phycol Res 55:91–102
Nagahama Y, Murray S, Tomaru A, Fukuyo Y (2011) Species boundaries in the toxic dinoflagellate Prorocentrum lima (Dinophyceae, Prorocentrales), based on morphological and phylogenetic characters. J Phycol 47:178–189
Nascimento SM, Mendes MCQ, Menezes M, Rodríguez F, Alves-de-Souza C, Branco S, Riobó P, Franco J, Nunes JMC, 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
Olsen DA, Nellis DW, Wood RS (1984) Ciguatera in the eastern Caribbean. Mar Fish Rev 46:13–18
Pottier I, Vernoux J-P, Lewis RJ (2001) Ciguatera fish poisoning in the Caribbean islands and western Atlantic. Rev Environ Contam Toxicol 168:99–141
Rasband WS (1997) ImageJ. National Institutes of Health. Bethesda, Maryland
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Saburova M, Chomérat N (2014) Ailadinium reticulatum gen. et sp. nov. (Dinophyceae), a new thecate, marine, sand-dwelling dinoflagellate from the northern Red Sea. J Phycol 50:1120–1136
Selina MS (2017) The morphology and seasonal dynamics of the potentially toxic microalga Prorocentrum foraminosum Faust 1993 (Dinophyta) in Peter the Great Bay, the Sea of Japan. Russ J Mar Biol 43:196–201. https://doi.org/10.1134/S1063074017030099
Stein F R (1878) Der Organismus der Infusionsthiere nach eigenen forschungen in systematischer reihenfolge bearbeitet. III. Abtheilung, I. Hälfte. In Engelmann, W. [Ed.] Die Naturgeschichte der Flagellaten Order Geisselinfusorien. Leipzig, Germany, pp 70–73
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Taylor FJR (1985) The distribution of the dinoflagellate Gambierdiscus toxicus in the eastern Caribbean. In: Gabrié C, Salvat B (eds). MNHN-EPHE, pp 423–428
Ten-Hage L, Turquet J, Quod JP, Puiseux-Dao S, Couté A (2000) Prorocentrum borbonicum sp. nov. (Dinophyceae), a new toxic benthic dinoflagellate from the southwestern Indian Ocean. Phycologia 39:296–301
Tester PA, Feldman RL, Nau AW, Kibler SR, Litaker RW (2010) Ciguatera fish poisoning and sea surface temperatures in the Caribbean Sea and the West Indies. Toxicon 56:698–710. https://doi.org/10.1016/j.toxicon.2010.02.026
Vernoux J-P (1988) La ciguatera dans l’île de Saint-Barthélémy: aspects épidémiologiques, toxicologiques et préventifs. Oceanol Acta 11:37–46
Zhang H, Li Y, Cen J, Wang H, Cui L, Dong Y, Lu S (2015) Morphotypes of Prorocentrum lima (Dinophyceae) from Hainan Island, South China Sea: morphological and molecular characterization. Phycologia 54:503–516. https://doi.org/10.2216/15-8.1
Acknowledgements
We thank Maurice Loir for his invaluable help and long-term collaboration, Maria A. Faust for her long-time encouragements and constant kindness, and Nicolas Gayet for critical point drying of the samples and support with SEM. This research received no specific grant from any funding agency, commercial or not-for-profit sector.
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Chomérat, N., Bilien, G. & Zentz, F. A taxonomical study of benthic Prorocentrum species (Prorocentrales, Dinophyceae) from Anse Dufour (Martinique Island, eastern Caribbean Sea). Mar Biodiv 49, 1299–1319 (2019). https://doi.org/10.1007/s12526-018-0913-6
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DOI: https://doi.org/10.1007/s12526-018-0913-6