Cite this paper:
CEN Jingyi, WANG Jianyan, HUANG Lifen, DING Guangmao, QI Yuzao, CAO Rongbo, CUI Lei, L� Songhui. Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019?[J]. HaiyangYuHuZhao, 2020, 38(3): 722-732

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

CEN Jingyi1,2, WANG Jianyan3, HUANG Lifen1,2, DING Guangmao4, QI Yuzao1, CAO Rongbo1,2, CUI Lei1,2, L� Songhui1,2
1 College of Life Science and Technology, Jinan University, Guangzhou 510632, China;
2 Key Laboratory of Aquatic Eutrophication and Control of Harmful Algae Blooms of Guangdong Higher Education Institutes, Guangzhou 510632, China;
3 Department of Science Research, Beijing Museum of Natural History, Beijing 100050, China;
4 Fujian Fishery Resources Monitoring Center, Fuzhou 350003, China
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.
Key words:    Karenia digitata|Karlodinium digitatum|harmful algal bloom|Ichthyotoxicity   
Received: 2019-07-08   Revised: 2019-07-30
Tools
PDF (2854 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by CEN Jingyi
Articles by WANG Jianyan
Articles by HUANG Lifen
Articles by DING Guangmao
Articles by QI Yuzao
Articles by CAO Rongbo
Articles by CUI Lei
Articles by L� Songhui
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.
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.
Brand L E, Campbell L, Bresnan E. 2012. Karenia:the biology and ecology of a toxic genus. Harmful Algae, 14(1):156-178.
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.
Cho C H. 1981. On the Gymnodinium red tide in Jinhae Bay.Korean Journal of Fisheries and Aquatic Sciences, 14(4):227-232.
Clément A, Seguel M, Arzul G, Guzmán 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.
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.
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.
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.
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.
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.
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.
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.
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.
Gómez F. 2012. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceánides, 27(1):65-140.
Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3):234-236.
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.
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.
Landsberg J H. 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10(2):113-390.
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.
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.
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.
Liu R Y. 2008. Checklist of Marine Biota of China Seas.Science Press, Beijing, China. p.177. (in Chinese)
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.
Lu S H, Hodgkiss I J. 2004. Harmful algal bloom causative collected from Hong Kong waters. Hydrobiologia, 512(1-3):231-238.
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.
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.
Partensky F, Vaulot D, Couté A, Sournia A. 1988. Morphological and nuclear analysis of the bloom-forming dinoflagellates Gyrodinium cf.aureolum andGymnodinium nagasakiense.Journal of Phycology, 24(3):408-415.
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.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3:bayesian phylogenetic inference under mixed models.Bioinformatics, 19(12):1 572-1 574.
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.
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.
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.
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.
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.
Tangen K. 1977. Blooms of Gyrodinium aureolum(Dinophygeae) in north European waters, accompanied by mortality in marine organisms. Sarsia, 63(2):123-133.
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.
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.
Wang J Y, Cen J Y, Li S, Lü S H, Moestrup Ø, 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.
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)
Yang Z B, Hodgkiss I J. 1999. Massive fish killing by Gyrodinium sp. Harmful Algae News, 18:4-5.
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.
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.