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Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019?

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Abstract

On May 24–29, 2019, a bloom occurring in Pingtan coastal areas of Fujian Province caused mass mortality of cage-cultured fish (Plectorhinchus cinctus and Pagrosomus major). During the bloom, two major causative organisms were present: Prorocentrum donghaiense (at a concentration of 1.46×107 cells/L) and an unknown naked dinoflagellate (4.58×106 cells/L). The naked dinoflagellate was isolated and cultured in this study, and its morphological features were examined using light microscopy and scanning electron microscopy. The large subunit (LSU) of the rRNA gene and the internal transcribed spacer (ITS) region of the naked dinoflagellate were also sequenced for field bloom samples and lab culture strains (PT-A and PT-B). On the basis of its morphological characteristics and molecular sequences, the unknown naked dinoflagellate was identified as Karlodinium digitatum. According to the phylogenetic analysis, the Karl. digitatum was most closely related to Karlodinium australe and Karlodinium armiger, and the three species clustered into a single clade of Karlodinium with bootstrap/posterior probability values of 95%/0.99 and 86%/0.99 inferred from LSU and ITS sequences, respectively. Karl. digitatum was first reported as Karenia digitata, a new harmful algal species bloomed in Hong Kong, China, in 1998. In present study, we gave a detailed morphological and phylogenetic description of Karl. digitatum and submitted the molecular sequences of this species to GenBank for the first time.

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon request.

References

  • Bergholtz T, Daugbjerg N, Moestrup Ø, Fernández-Tejedor M. 2006. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. Journal of Phycology, 42(1): 170–193.

    Article  Google Scholar 

  • Botes L, Smit A J, Cook P A. 2003. The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae, 2(4): 247–259.

    Article  Google Scholar 

  • Brand L E, Campbell L, Bresnan E. 2012. Karenia: the biology and ecology of a toxic genus. Harmful Algae, 14(1): 156–178.

    Article  Google Scholar 

  • Chang F H, Chiswell S M, Uddstrom M J. 2001. Occurrence and distribution of Karenia brevisulcata (Dinophyceae) during the 1998 summer toxic outbreaks on the central east coast of New Zealand. Phycologia, 40(3): 215–221.

    Article  Google Scholar 

  • Cho C H. 1981. On the Gymnodinium red tide in Jinhae Bay. Korean Journal of Fisheries and Aquatic Sciences, 14(4): 227–232.

    Google Scholar 

  • Clément A, Seguel M, Arzul G, Guzman L, Alarcón C. 2001. A widespread outbreak of a haemolytic, ichthyotoxic Gymnodinium sp. in southern Chile. In: Hallegraeff G M, Blackburn S I, Bolch C J, Lewis R J eds. Harmful algal blooms 2000. Intergovernmental Oceanographic Commission, UNESCO, Paris. p.66–69.

    Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø. 2000, Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia, 39(4): 302–317.

    Article  Google Scholar 

  • de Salas M F, Bolch C J S, Botes L, Nash G, Wright S W, Hallegraeff G M. 2003. Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. Journal of Phycology, 39(6): 1 233–1 246.

    Article  Google Scholar 

  • de Salas M F, Bolch C J S, Hallegraeff G M. 2004. Karenia umbella sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia, 43(2): 166–175.

    Article  Google Scholar 

  • de Salas M F, Bolch C J S, Hallegraeff G M. 2005. Karlodinium australe sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic unarmoured dinoflagellate from lagoonal habitats of south-eastern Australia. Phycologia, 44(6): 640–650.

    Article  Google Scholar 

  • de Salas M F, Laza-Martínez A, Hallegraeff G M. 2008. Novel unarmored dinoflagellates from the toxigenic family Kareniaceae (Gymnodiniales): five new species of Karlodinium and one new Takayama from the Australian sector of the Southern Ocean. Journal of Phycology, 44(1): 241–257.

    Article  Google Scholar 

  • Fujian Provincial Department of Ocean and Fisheries, China. 2019. Red tide disaster information in Fujian Province (No. 019). http://hyyyj.fujian.gov.cn/xxgk/tzgg/201905/t20190525_4885308.htm

  • Gentien P. 1998. Bloom dynamics and ecophysiology of the Gymnodinium mikimotoi species complex. In: Anderson D M, Cembella A D, Hallegraeff G M eds. Physiological Ecology of Harmful Algal Blooms. Springer, Berlin. p.155–173.

    Google Scholar 

  • GEOHAB. 2001. Global Ecology and Oceanography of Harmful Algal Blooms. In: Gilbert P M, Pitcher G eds. Science Plan. SCOR- IOC (UNESCO), Baltimore and Paris. 86p.

    Google Scholar 

  • Gómez F, Nagahama J, Takayama H, Furuya K. 2005. Is Karenia a synonym of Asterodinium-Brachidinium (Gymnodiniales, Dinophyceae)? Acta Botanica Croatica, 64(2): 263–274.

    Google Scholar 

  • Gómez F. 2012. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceánides, 27(1): 65–140.

    Google Scholar 

  • Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3): 234–236.

    Article  Google Scholar 

  • Haywood A J, Steidinger K A, Truby E W, Bergquist P R, Bergquist P L, Adamson J, Mackenzie L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. Journal of Phycology, 40(1): 165–179.

    Article  Google Scholar 

  • Heil C A, Steidinger K A. 2009. Monitoring, management, and mitigation of Karenia blooms in the eastern Gulf of Mexico. Harmful Algae, 8(4): 611–617.

    Article  Google Scholar 

  • Landsberg J H. 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10(2): 113–390.

    Article  Google Scholar 

  • Lee F W, Ho K C, Mak Y L, Lo C L. 2011. Authentication of the proteins expression profiles (PEPs) identification methodology in a bloom of Karenia digitata, the most damaging harmful algal bloom causative agent in the history of Hong Kong. Harmful Algae, 12: 1–10.

    Article  Google Scholar 

  • Lenaers G, Maroteaux L, Michot B, Herzog M. 1989. Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. Journal of Molecular Evolution, 29(1): 40–51.

    Article  Google Scholar 

  • Li X D, Yan T, Lin J N, Yu R C, Zhou M J. 2017. Detrimental impacts of the dinoflagellate Karenia mikimotoi in Fujian coastal waters on typical marine organisms. Harmful Algae, 61: 1–12.

    Article  Google Scholar 

  • Liu R Y. 2008. Checklist of Marine Biota of China Seas. Science Press, Beijing, China. p.177. (in Chinese)

    Google Scholar 

  • Lu D D, Qi Y Z, Gu H F, Dai X F, Wang H X, Gao Y H, Shen P P, Zhang Q C, Yu R C, Lu S H. 2014. Causative species of harmful algal blooms in Chinese coastal waters. Algological Studies, 145–146(1): 145–168.

    Article  Google Scholar 

  • Lu S H, Hodgkiss I J. 2004. Harmful algal bloom causative collected from Hong Kong waters. Hydrobiologia, 512(1–3): 231–238.

    Article  Google Scholar 

  • Luo Z H, Wang L, Chan L, Lu S H, Gu H H. 2018. Karlodinium zhouanum, a new dinoflagellate species from China, and molecular phylogeny of Karenia digitata and Karenia longicanalis (Gymnodiniales, Dinophyceae). Phycologia, 57(4): 401–412.

    Article  Google Scholar 

  • Oda M. 1935. Gymnodinium mikimotoi Miyake et Kominami n. sp. (MS) and the influence of copper sulfate on the red tide. Dobutsugaku Zassh, 47: 35–48.

    Google Scholar 

  • Partensky F, Vaulot D, Couté A, Sournia A. 1988. Morphological and nuclear analysis of the bloom-forming dinoflagellates Gyrodinium cf. aureolum and Gymnodinium nagasakiense. Journal of Phycology, 24(3): 408–415.

    Article  Google Scholar 

  • Rasmussen S A, Binzer S B, Hoeck C, Meier S, de Medeiros L S, Andersen N G, Place A, Nielsen K F, Hansen P J, Larsen T O. 2017. Karmitoxin: an amine-containing polyhydroxy-polyene toxin from the marine dinoflagellate Karlodinium armiger. Journal of Natural Products, 80(5): 1 287–1 293.

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1 572–1 574.

    Article  Google Scholar 

  • 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): 999–1 011.

    Article  Google Scholar 

  • SOAC 2005–2017 (State Oceanic Administration, China). The National Marine Economic Statistics Bulletin, China Oceanic Information Network (2005–2017). http://m.lc.mlr.gov.cn/sj/sjfw/hy/gbgg/zghyzhgb/. (in Chinese)

  • Steidinger K A, Wolny J L, Haywood A J. 2008. Identification of kareniaceae (Dinophyceae) in the gulf of Mexico. Nova Hedwigia, 133: 269–284.

    Google Scholar 

  • Stern R F, Andersen R A, Jameson I, Küpper F C, Coffroth M A, Vaulot D, Le Gall F, Véron B, Brand J J, Skelton H, Kasai F, Lilly E L, Keeling P J. 2012. Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS One, 7(8): e42780.

    Article  Google Scholar 

  • Takayama H, Adachi R. 1984. Gymnodinium nagasakiense sp. nov., a red-tide forming dinophyte in the adjacent waters of Japan. Bulletin of Plankton Society of Japan, 31(1): 7–14.

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12): 2 725–2 729.

    Article  Google Scholar 

  • Tangen K. 1977. Blooms of Gyrodinium aureolum (Dinophygeae) in north European waters, accompanied by mortality in marine organisms. Sarsia, 63(2): 123–133.

    Article  Google Scholar 

  • Tester P A, Steidinger K A. 1997. Gymnodinium breve red tide blooms: Initiation, transport, and consequences of surface circulation. Limnology and Oceanography, 42(5): 1 039–1 051.

    Article  Google Scholar 

  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24): 4 876–4 882.

    Article  Google Scholar 

  • Wang J Y, Cen J Y, Li S, Lü S H, Moestrup Ó, Chan K K, Jiang T, Lei X D. 2018. A re-investigation of the bloom-forming unarmored dinoflagellate Karenia longicanalis (syn. Karenia umbella) from Chinese coastal waters. Journal of Oceanology and Limnology, 36(6): 2 202–2 215.

    Google Scholar 

  • Xu C Y, Huang M Z, Du Q. 2010. Ecological characteristics of important red tide species in Fujian coastal waters. Journal of Oceanography in Taiwan Strait, 29(3): 434–441. (in Chinese with English abstract)

    Google Scholar 

  • Yang Z B, Hodgkiss I J. 1999. Massive fish killing by Gyrodinium sp. Harmful Algae News, 18: 4–5.

    Google Scholar 

  • Yang Z B, Hodgkiss I J. 2004. Hong Kong’s worst “red tide”-causative factors reflected in a phytoplankton study at Port Shelter station in 1998. Harmful Algae, 3(2): 149–161.

    Article  Google Scholar 

  • Yang Z B, Takayama H, Matsuoka K, Hodgkiss I J. 2000. Karenia digitata sp. nov. (Gymnodiniales, Dinophyceae), a new harmful algal bloom species from the coastal waters of west Japan and Hong Kong. Phycologia, 39(6): 463–470.

    Article  Google Scholar 

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Acknowledgment

Special appreciation is expressed to Prof. Moestrup of the University of Copenhagen for helpful discussions regarding the species identification. We also sincerely thank Dr. ZHEN Yu of the Ocean University of China for his assistance with the molecular data analysis.

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Correspondence to Songhui Lü.

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Supported by the National Key R&D Program of China (No. 2017YFC1404301), the National Natural Science Foundation of China (No. 41606175), and the Beijing Natural Science Foundation (No. 8194059)

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Cen, J., Wang, J., Huang, L. et al. Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019?. J. Ocean. Limnol. 38, 722–732 (2020). https://doi.org/10.1007/s00343-019-9178-6

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