Abstract
The potentially toxic dinoflagellate genera Gambierdiscus, Ostreopsis, Coolia, previously considered inhabitants of the tropical and subtropical zones, have expanded their ranges to temperate latitudes in recent decades, presumably due to ongoing global warming. Coolia species are widely distributed in the Indo-Pacific. Until recently, the northernmost known point of the Coolia distribution range in the Pacific region has been the eastern coast of the Korean Peninsula. In this paper, we report, for the first time, the presence of the genus Coolia in Pacific waters of Russia. This is also the first finding of Coolia in waters with below-zero winter temperatures. The morphology of the Russian strain of Coolia malayensis isolated from Peter the Great Bay, Sea of Japan, matches the original description of the Malaysian strain and is similar to the morphology of other strains from the Pacific region A phylogenetic analysis has clustered the Russian strain with the clade of C. malayensis, showing a 100 % similarity with the strains isolated from South Korea, New Zealand, and Malaysia and with the strains from the Canary Islands. Further observations are needed to clarify if C. malayensis is acclimated, or not, in this part of the Sea of Japan.
Funding source: Federal Service for Hydrometeorology and Environmental Monitoring of the Russian Federation
Award Identifier / Grant number: agreement no. 169-15-2023-002
Acknowledgments
Special thanks are due to Evgeny Shvetsov for his help in proofreading the English of the manuscript.
-
Research ethics: Not applicable.
-
Informed consent: Not applicable.
-
Author contributions: M.S.S.: conceptualization sampling, microscopy, original draft preparation and writing; K.V.E.: molecular work, phylogenetic analysis, writing. All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Use of Large Language Models, AI and Machine Learning Tools: None declared.
-
Conflict of interest: The authors declare no conflicts of interest regarding this article.
-
Research funding: This study was supported by the Federal Service for Hydrometeorology and Environmental Monitoring of the Russian Federation, agreement no. 169-15-2023-002.
-
Data availability: Not applicable.
References
Abdennadher, M., Zouari, A.B., Medhioub, W., Penna, A., and Hamza, A. (2021). Characterization of Coolia spp. (Gonyaucales, Dinophyceae) from Southern Tunisia: first record of Coolia malayensis in the Mediterranean Sea. Algae 36: 175–193, https://doi.org/10.4490/algae.2021.36.6.2.Search in Google Scholar
Akasaka, K., Shichijyukari, S., Matsuoka, S., Murata, M., Meguro, H., and Ohrui, H. (2000). Absolute configuration of a Ceramide with novel branched-chain fatty acid isolated from the epiphytic dinoflagellate, Coolia monotis. Biosci. Biotechnol. Biochem. 64: 1842–1846, https://doi.org/10.1271/bbb.64.1842.Search in Google Scholar PubMed
Aligizaki, K., Katikou, P., Milandri, A., and Diogène, J. (2011). Occurrence of palytoxin-group toxins in seafood and future strategies to complement the present state of the art. Toxicon 57: 390–399, https://doi.org/10.1016/j.toxicon.2010.11.014.Search in Google Scholar PubMed
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403–410, https://doi.org/10.1016/s0022-2836-05-80360-2.Search in Google Scholar
Anisimova, M., Gil, M., Dufayard, J.F., Dessimoz, C., and Gascuel, O. (2011). Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst. Biol. 60: 685–699, https://doi.org/10.1093/sysbio/syr041.Search in Google Scholar PubMed PubMed Central
Balech, E. (1980). On the thecal morphology of dinoflagellates with special emphasis on circular and sulcal plates. Ann. Centro Cienc. Mar. Limnol. Univ. Nal. Auton. Mexico 7: 57–68.Search in Google Scholar
Berdalet, E., Tester, P.A., Chinain, M., Fraga, S., Lemee, R., Litaker, W., Penna, A., Usup, G., Vila, M., and Zingone, A. (2017). Harmful algal blooms in benthic systems: recent progress and future research. Oceanography 30: 36–45, https://doi.org/10.5670/oceanog.2017.108.Search in Google Scholar
Danchenkov, M.A. (2023). Analiticheskii obzor. Okeanograficheskie usloviya zaliva Petra Velikogo po dannym ekspedicionnyh nablyudenii v 2021–2022 gg. (Oceanographic conditions in Peter the Great Bay according to data of observations during expeditions in 2021–2022: an analytical review), Available at: http://ferhri.org/images/stories/FERHRI/science/zalivPV/Obzor2022/oceanography_22.pdf.Search in Google Scholar
David, H., Laza-Martínez, A., Miguel, I., and Orive, E. (2014). Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) on the Atlantic coast of the Iberian Peninsula. Phycologia 53: 342–352, https://doi.org/10.2216/13-214.1.Search in Google Scholar
de Queiroz Mendes, M., de Castro Nunes, J., Fraga, S., Rodríguez, F., Franco, J., Riobó, P., Branco, S., and Menezes, M. (2019). Morphology, molecular phylogeny and toxicology of Coolia and Prorocentrum strains isolated from the tropical South Western Atlantic Ocean. Bot. Mar. 62: 125–140, https://doi.org/10.1515/bot-2018-0053.Search in Google Scholar
Durando, P., Ansaldi, F., Oreste, P., Moscatelli, P., Marensi, L., Grillo, C., Gasparini, R., and Icardi, G. (2007). Ostreopsis ovata and human health: epidemiological and clinical features of respiratory syndrome outbreaks from a two-year syndromic surveillance, 2005–06, in north-west Italy. Euro. Surveill. 12: E070607, https://doi.org/10.2807/esw.12.23.03212-en.Search in Google Scholar PubMed
Faust, M.A. (1992). Observations on the morphology and sexual reproduction of Coolia monotis (Dinophyceae). J. Phycol. 28: 94–104, https://doi.org/10.1111/j.0022-3646.1992.00094.x.Search in Google Scholar
Fleming, L.E., Baden, D.G., Bean, J.A., Weisman, R., and Blythe, D.G. (1998). Seafood toxin diseases: issues in epidemiology and community outreach. In: Reguera, B., Blanco, J., Fernandez, M.L., and Wyatt, T. (Eds.). Harmful algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Paris, pp. 245–248.Search in Google Scholar
Golovan, O.A. and Malyutina, M.V. (2010). Isopoda. In: Chernyshev, A.V. (Ed.). Biota of the Russian waters of the Sea of Japan, Vol. 9, part 1. Dalnauka, Vladivostok, pp. 1–357, (In Russian).Search in Google Scholar
Gómez, F., Qiu, D., Otero-Morales, E., Lopes, R.M., and Lin, S. (2016). Circumtropical distribution of the epiphytic dinoflagellate Coolia malayensis (Dinophyceae): morphology and molecular phylogeny from Puerto Rico and Brazil. Phycol. Res. 64: 194–199, https://doi.org/10.1111/pre.12134.Search in Google Scholar
Granéli, E., Vidyarathna, N.K., Funari, E., Cumaranatunga, P., and Scenati, R. (2011). Can increases in temperature stimulate blooms of the toxic benthic dinoflagellate Ostreopsis ovata? Harmful Algae 10: 165–172, https://doi.org/10.1016/j.hal.2010.09.002.Search in Google Scholar
Guillard, R.R.L. (1975). Culture of phytoplankton for feeding marine invertebrates. In: Smith, W.L., and Chanley, M.H. (Eds.). Culture of marine invertebrate animals. Plenum Press, New York, pp. 26–60.10.1007/978-1-4615-8714-9_3Search in Google Scholar
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59: 307–321, https://doi.org/10.1093/sysbio/syq010.Search in Google Scholar PubMed
Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q., and Vinh, L.S. (2018). UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35: 518–522, https://doi.org/10.1093/molbev/msx281.Search in Google Scholar PubMed PubMed Central
Holmes, M.J., Lewis, R.J., Jones, A., and Wong Hoy, A. (1995). Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins 3: 355–362, https://doi.org/10.1002/nt.2620030506.Search in Google Scholar PubMed
Hoppenrath, M., Chomérat, N., Horiguchi, T., Murray, S.A., and Rhodes, L. (2023). Marine benthic dinoflagellates – their relevance for science and society, 2nd ed. Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main.Search in Google Scholar
Hyung, J.H., Moon, S.J., Lee, H., and Park, J. (2024). First report of Coolia palmyrensis in Korea: seasonal and spatial distribution of C. palmyrensis and C. malayensis in Korean coastal waters. Front. Mar. Sci. 11: 1469015, https://doi.org/10.3389/fmars.2024.1469015.Search in Google Scholar
Jeong, H.J., Yih, W., Kang, N.S., Lee, S.Y., Yoon, E.Y., Yoo, Y.D., Kim, H.S., and Kim, J.H. (2012). First report of the epiphytic benthic dinoflagellates Coolia canariensis and Coolia malayensis in the waters off Jeju Island, Korea: morphology and rDNA sequences. J. Eukaryot. Microbiol. 59: 114–133, https://doi.org/10.1111/j.1550-7408.2012.00610.x.Search in Google Scholar PubMed
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A., and Jermiin, L.S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14: 587–589, https://doi.org/10.1038/nmeth.4285.Search in Google Scholar PubMed PubMed Central
Karafas, S., York, R., and Tomas, C. (2015). Morphological and genetic analysis of the Coolia monotis species complex with the introduction of two new species, Coolia santacroce sp. nov. and Coolia palmyrensis sp. nov. (Dinophyceae). Harmful Algae 46: 18–33, https://doi.org/10.1016/j.hal.2015.05.002.Search in Google Scholar
Katoh, K., Rozewicki, J., and Yamada, K.D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20: 1160–1166, https://doi.org/10.1093/bib/bbx108.Search in Google Scholar PubMed PubMed Central
Kwak, M.T., Seo, G.H., Cho, Y.K., Kim, B.G., You, S.H., and Seo, J.W. (2015). Long-term comparison of satellite and in-situ sea surface temperatures around the Korean Peninsula. Ocean Sci. J. 50: 109–117, https://doi.org/10.1007/s12601-015-0009-1.Search in Google Scholar
Larsson, M.E., Smith, K.F., and Doblin, M.A. (2019). First description of the environmental niche of the epibenthic dinoflagellate species Coolia palmyrensis, C. malayensis, and C. tropicalis (Dinophyceae) from eastern Australia. J. Phycol. 55: 565–577, https://doi.org/10.1111/jpy.12833.Search in Google Scholar PubMed
Leaw, C.P., Lim, P.T., Cheng, K.W., Ng, B.K., and Usup, G. (2010). Morphology and molecular characterization of a new species of thecate benthic dinoflagellate, Coolia malayensis sp. nov. (Dinophyceae). J. Phycol. 46: 162–171, https://doi.org/10.1111/j.1529-8817.2009.00778.x.Search in Google Scholar
Leaw, C.P., Tan, T.H., Lim, H.C., Teng, S.T., Yong, H.L., Smith, K.F., Rhodes, L., Wolf, M., Holland, W.C., Vandersea, M.W., et al.. (2016). New scenario for speciation in the benthic dinoflagellate genus Coolia (Dinophyceae). Harmful Algae 55: 137–149, https://doi.org/10.1016/j.hal.2016.02.010.Search in Google Scholar PubMed
Letunic, I. and Bork, P. (2021). Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucl. Acids Res. 49: W293–W296, https://doi.org/10.1093/nar/gkab301.Search in Google Scholar PubMed PubMed Central
Leung, P.T.Y., Yan, M., Yiu, S.K.F., Lam, V.T.T., Ip, J.C.H., Au, M.W.Y., Chen, C.Y., Wai, T.C., and Lam, P.K.S. (2017). Molecular phylogeny and toxicity of harmful benthic dinoflagellates Coolia (Ostreopsidaceae, Dinophyceae) in a sub-tropical marine ecosystem: the first record from Hong Kong. Mar. Poll. Bull. 124: 878–889, https://doi.org/10.1016/j.marpolbul.2017.01.017.Search in Google Scholar PubMed
Lim, A.S. and Jeong, H.J. (2021). Benthic dinoflagellates in Korean waters. Algae 36: 91–109, https://doi.org/10.4490/algae.2021.36.5.31.Search in Google Scholar
Lotsiya severo-zapadnogo berega Yaponskogo morya. Ot reki Tumannaya do mysa Belkina (Northwestern Sea of Japan Coast Pilot. From the Tumen River to Cape Belkin). (2017). Gl. Upr. Navig. Kartogr.: Moscow, no. 1401. (In Russian)Search in Google Scholar
Lutaenko, K.A. and Noseworthy, R.G. (2012). Catalogue of the living bivalvia of the continental coast of the Sea of Japan (East Sea). Dalnauka, Vladivostok.Search in Google Scholar
Mangialajo, L., Bertolotto, R., Cattaneo-Vietti, R., Chiantore, M., Grillo, C., Lemee, R., Melchiorre, N., Moretto, P., Povero, P., and Ruggieri, N. (2008). The toxic benthic dinoflagellate Ostreopsis ovata: quantification of proliferation along the coastline of Genoa, Italy. Mar. Poll. Bull. 56: 1209–1214, https://doi.org/10.1016/j.marpolbul.2008.02.028.Search in Google Scholar PubMed
Meunier, A. (1919). Microplancton de la Mer Flamande. 3. Les Péridiniens. Mem. Mus. R. Hist. Nat., Bruxelles 8: 3–116.Search in Google Scholar
Morales-Montesinos, I.B., Rios, M.Y., Ocampo-Acuña, Y.D., Esquivel-Rodríguez, B., Bustos-Brito, C., Osorio-Ramírez, M.d.C., Durán-Riveroll, L.M., and González-Maya, L. (2025). The Benthic dinoflagellate Coolia malayensis (Dinophyceae) produces an array of compounds with antineoplastic activity in cells of tumor origin. Mar. Drugs 23: 127, https://doi.org/10.3390/md23030127.Search in Google Scholar PubMed PubMed Central
Mohammad-Noor, N., Moestrup, Ø., Lundholm, N., Fraga, S., Adam, A., Holmes, M.J., and Saleh, E. (2013). Autecology and phylogeny of Coolia tropicalis and Coolia malayensis (Dinophyceae), with emphasis on taxonomy of C. tropicalis based on light microscopy, scanning electron microscopy and LSU rDNA. J. Phycol. 49: 536–545, https://doi.org/10.1111/jpy.12062.Search in Google Scholar PubMed
Momigliano, P., Sparrow, L., Blair, D., and Heimann, K. (2013). The diversity of Coolia spp. (Dinophyceae Ostreopsidaceae) in the central great Barrier Reef region. PLoS One 8: e79278, https://doi.org/10.1371/journal.pone.0079278.Search in Google Scholar PubMed PubMed Central
Morquecho, L., Gárate-Lizárraga, I., and Gu, H. (2022). Morphological and molecular characterization of the genus Coolia (Dinophyceae) from Bahía de La Paz, southwest Gulf of California. Algae 37: 185–204.10.4490/algae.2022.37.9.2Search in Google Scholar
Mussai, P., Larsen, J., Alrefaei, A.F., Rajeshkumar, K.C., and Jeewon, R. (2025). Morpho-taxonomy and molecular characterization of Coolia canariensis S. Fraga and Ostreopsis ovata Fukuyo (Ostreopsidaceae, Dinophyceae) from Mauritius (Indian Ocean) marine coastal waters. Diversity 17: 154, https://doi.org/10.3390/d17030154.Search in Google Scholar
Nascimento, S.M., da Silva, R.A., Oliveira, F., Fraga, S., and Salgueiro, F. (2019). Morphology and molecular phylogeny of Coolia tropicalis, Coolia malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae) isolated from Brazil. Eur. J. Phycol. 54: 484–496, https://doi.org/10.1080/09670262.2019.1599449.Search in Google Scholar
Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B.Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 32: 268–274, https://doi.org/10.1093/molbev/msu300.Search in Google Scholar PubMed PubMed Central
Orlova, T.Y., Aleksanin, A.I., Lepskaya, E.V., Efimova, K.V., Selina, M.S., Morozova, T.V., Stonik, I.V., Kachur, V.A., Karpenko, A.A., Vinnikov, K.A., et al.. (2022). A massive bloom of Karenia species (Dinophyceae) off the Kamchatka coast, Russia, in the fall of 2020. Harmful Algae 120: 102337, https://doi.org/10.1016/j.hal.2022.102337.Search in Google Scholar PubMed
Phua, Y.H., Roy, M.C., Lemer, S., Husnik, F., and Wakeman, K.C. (2021). Diversity and toxicity of Pacific strains of the benthic dinoflagellate Coolia (Dinophyceae), with a look at the Coolia canariensis species complex. Harmful Algae 109: 102120, https://doi.org/10.1016/j.hal.2021.102120.Search in Google Scholar PubMed
Rhodes, L. (2011). World-wide occurrence of the toxic dinoflagellate genus Ostreopsis. Schmidt. Toxicon 57: 400–407, https://doi.org/10.1016/j.toxicon.2010.05.010.Search in Google Scholar PubMed
Rhodes, L.L., Smith, K.F., Gimenez, P.G., Adamson, J.E., Harwood, T., and Munday, R. (2014). Epiphytic dinoflagellates in sub-tropical New Zealand, in particular the genus Coolia Meunier. Harmful Algae 34: 36–41, https://doi.org/10.1016/j.hal.2014.02.004.Search in Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574, https://doi.org/10.1093/bioinformatics/btg180.Search in Google Scholar PubMed
Selina, M.S. and Levchenko, E.V. (2011). Species composition and morphology of dinoflagellates (Dinophyta) of epiphytic assemblages of Peter the great bay in the Sea of Japan. Russ. J. Mar. Biol. 37: 23–32, https://doi.org/10.1134/s1063074011010135.Search in Google Scholar
Scholin, C.A., Herzog, M., and Anderson, D.M. (1994). Identification of group and strain specific genetic markets for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30: 999–1011.10.1111/j.0022-3646.1994.00999.xSearch in Google Scholar
Selina, M.S. (1993). Ensiculifera carinata Matsuoka, Kobayashi et Gains (Dinophyta) ‒ a new species for the seas of Russia. Algologia 3: 78–83, (in Russian).Search in Google Scholar
Selina, M.S., Morozova, T.V., Vyshkvartsev, D.I., and Orlova, T.Y. (2014). Seasonal dynamics and spatial distribution of epiphytic dinoflagellates in Peter the Great Bay (Sea of Japan) with special emphasis on Ostreopsis species. Harmful Algae 32: 1–10, https://doi.org/10.1016/j.hal.2013.11.005.Search in Google Scholar
Selina, M.S. and Orlova, T.Y. (2010). First occurrence of the genus Ostreopsis (Dinophyceae) in the Sea of Japan. Bot. Mar. 53: 243–249, https://doi.org/10.1515/bot.2010.033.Search in Google Scholar
Selina, M.S., Simakova, N.K., and Yasnetskaya, L.V. (1992). Gymnodinium nagasakiense Takayama et Adachi (Dinophyta) in Peter the Great Bay (Sea of Japan). Algologiya 2: 51–55, (in Russian).Search in Google Scholar
Shah, M.M.R., An, S.J., and Lee, J.B. (2013a). Presence of benthic dinoflagellates around coastal waters of Jeju Island including newly recorded species. J. Ecol. Environ. 36: 347–370, https://doi.org/10.5141/ecoenv.2013.347.Search in Google Scholar
Shah, M.M.R., An, S.J., and Lee, J.B. (2013b). Seasonal abundance of epiphytic dinoflagellates around coastal waters of Jeju Island, Korea. J. Mar. Sci. Technol. 21: 156–165.Search in Google Scholar
Shah, M.M.R., Samarakoon, K.W., Ko, J.Y., Chaminda Lakmal, H.H., Lee, J.H., An, S.J., Jeon, Y.J., and Lee, J.B. (2014). Potentiality of benthic dinoflagellate cultures and screening of their bioactivities in Jeju Island, Korea. Afr. J. Biotechnol. 13: 792–805, https://doi.org/10.5897/ajb2013.13250.Search in Google Scholar
Shears, N.T. and Ross, P.M. (2009). Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 8: 916–925, https://doi.org/10.1016/j.hal.2009.05.003.Search in Google Scholar
Sokolovsky, A.S., Sokolovskaya, T.G., and Yakovlev, Y.M. (2011). Fishes of the Peter the Great Bay, 2nd ed. Dalnauka, Vladivostok, (In Russian).Search in Google Scholar
Tubaro, A., Durando, P., Del Favero, G., Ansaldi, F., Icardi, G., Deeds, J., and Sosa, S. (2011). Case definitions for human poisonings postulated to palytoxins exposure. Toxicon 57: 478–495, https://doi.org/10.1016/j.toxicon.2011.01.005.Search in Google Scholar PubMed
Uribe, E., Álvarez, G., Cárcamo, C., Díaz, P.A., Rengel, J., and Blanco, J. (2023). First report of epiphytic dinoflagellate Coolia malayensis (Dinophyceae) in the southeastern Pacific Ocean. J. Phycol. 59: 725–737, https://doi.org/10.1111/jpy.13351.Search in Google Scholar PubMed
Verma, A., Hoppenrath, M., Smith, K.F., Murray, J.S., Harwood, D.T., Hosking, T., Rongo, T., Rhodes, L.L., and Murray, S.A. (2023). Ostreopsis Schmidt and Coolia Meunier (Dinophyceae, Gonyaulacales) from Cook Islands and Niue (South Pacific Ocean), including description of Ostreopsis tairoto sp. nov. Sci. Rep. 13: 3110, https://doi.org/10.1038/s41598-023-29969-z.Search in Google Scholar PubMed PubMed Central
Wakeman, К.С., Yamaguchi, A., Roy, M.C., and Jenke-Kodama, H. (2015). Morphology, phylogeny and novel chemical compounds from Coolia malayensis (Dinophyceae) from Okinawa, Japan. Harmful Algae 44: 8–19, https://doi.org/10.1016/j.hal.2015.02.009.Search in Google Scholar
Zhang, H., Lü, S., Cen, J., Li, Y., Li, Q., and Wu, Z. (2021). Morphology and molecular phylogeny of three species of Coolia (Dinophyceae) from Hainan Island, South China sea. J. Oceanol. Limnol. 39: 1020–1032.10.1007/s00343-020-9326-zSearch in Google Scholar
© 2025 Walter de Gruyter GmbH, Berlin/Boston