Cite this paper:
WANG Jianyan, CEN Jingyi, LI Si, LÜ Songhui, MOESTRUP Øjvind, CHAN Kin-Ka, JIANG Tao, LEI Xiangdong. A re-investigation of the bloom-forming unarmored dinoflagellate Karenia longicanalis (syn. Karenia umbella) from Chinese coastal waters[J]. HaiyangYuHuZhao, 2018, 36(6): 2202-2215

A re-investigation of the bloom-forming unarmored dinoflagellate Karenia longicanalis (syn. Karenia umbella) from Chinese coastal waters

WANG Jianyan1, CEN Jingyi2,3, LI Si2,3, LÜ Songhui2,3, MOESTRUP Øjvind4, CHAN Kin-Ka5, JIANG Tao6, LEI Xiangdong7
1 Department of Science Research, Beijing Museum of Natural History, Beijing 100050, China;
2 College of Life Science and Technology, Jinan University, Guangzhou 510632, China;
3 Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China;
4 Marine Biological Section, Department of Biology, University of Copenhagen, Universitetsparken 4, DK-2100 Copenhagen Ø, Denmark;
5 School of Science & Technology, Open University of Hong Kong, 999077 Kowloon, Hong Kong, China;
6 Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
7 Wenzhou Marine Environmental Monitoring Center Station, State Oceanic Administration, Wenzhou 325013, China
The dinoflagellate genus Karenia is known for recurrent harmful blooms worldwide. However, species diversity of the genus is generally overlooked owing to the difficulty of identifying small unarmored dinoflagellates. We have established four clonal cultures of Karenia longicanalis isolated from the type locality, Hong Kong harbor (strain HK01) and other three locations along the Chinese coasts (strains YB01, DT01, and NJ01). The morphology of the strain was studied by light and scanning electron microscopy (LM and SEM) and the pigment composition analyzed by high-performance liquid chromatography. We provide the first molecular data of K. longicanalis based on the large subunit (LSU) rRNA gene sequence and internal transcribed spacer (ITS). The four strains showed identical LSU rDNA sequences with a similarity of 99.4% to the holotype of Karenia umbella (strain KUTN05) from Australia. In the ITS phylogeny, the sequence of K. umbella branched between the Chinese strains of K. longicanalis. A careful comparison of the morphology of K. longicanalis and K. umbella reveals the similarity in the diagnostic characters. Differences may appear due to the sample treatment for SEM. We conclude that K. umbella is a junior synonym of K. longicanalis.
Key words:    harmful algal blooms (HABs)|phytoplankton|morphology|phylogeny|large subunit (LSU) rRNA|internal transcribed spacer (ITS)   
Received: 2017-06-28   Revised:
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Articles by WANG Jianyan
Articles by CEN Jingyi
Articles by LI Si
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Articles by MOESTRUP Øjvind
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Articles by JIANG Tao
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Al-Kandari M A, Highfield A C, Hall M J, Hayes P, Schroeder D C. 2011. Molecular tools separate harmful algal bloom species, Karenia mikimotoi, from different geographical regions into distinct sub-groups. Harmful Algae, 2011, 10(6):636-643.
Bergholtz T, Daugbjerg N, Moestrup Ø, Fernández-Tejedor M. 2005. 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, Sym S D, Pitcher G C. 2003. Karenia cristata sp. nov.and Karenia bicuneiformis sp. nov. (Gymnodiniales, Dinophyceae):two new Karenia species from the South African coast. Phycologia, 42(6):563-571.
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, Charleston W A G, McKenna P B, Clowes C D, Wilson G J, Broady P A. 2012. Phylum Myzozoa:dinoflagellates, perkinsids, ellobiopsids, sporozoans. In:Gordon D P Ed. New Zealand inventory of biodiversity:Vol. 3:Kingdoms Bacteria, Protozoa, Chromista, Plantae, Fungi. Canterbury University Press, Christchurch, New Zealand. p.175-216.
Chang F H. 1999. Gymnodinium brevisulcatum sp. nov.(Gymnodiniales, Dinophyceae), a new species isolated from the 1998 summer toxic bloom in Wellington Harbour, New Zealand. Phycologia, 38(5):377-384.
Connell L B. 2000. Nuclear ITS region of the alga Heterosigma akashiwo (Chromophyta:Raphidophyceae) is identical in isolates from Atlantic and Pacific basins. Marine Biology, 136(6):953-960.
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. 2004a. 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. 2004b. Karenia asterichroma sp. nov. (Gymnodiniales, Dinophyceae), a new dinoflagellate species associated with finfish aquaculture mortalities in Tasmania, Australia.Phycologia, 43(5):624-631.
de Salas M F, Laza-Martínez A, Hallegraeff G M. 2008. Novel unarmored dinoflagellates from the toxigenic family Kareniaceae (Gymnodiales):five new species of Karlodinium and one new Takayama from the Australian sector of the Southern Ocean. Journal of Phycology, 44(1):241-257.
de Salas M F, Rhodes L L, Mackenzie L A, Adamson J E. 2005.Gymnodinoid genera Karenia and Takayama(Dinophyceae) in New Zealand coastal waters. New Zealand Journal of Marine and Freshwater Research, 39(1):135-139.
Fowler N, Tomas C, Baden D, Campbell L, Bourdelais A. 2015. Chemical analysis of Karenia papilionacea.Toxicon, 101:85-91.
Garcés E, Fernandez M, Penna A, Van Lenning K, Gutierrez A, Camp J, Zapata M. 2006. Characterization of NW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. Journal of Phycology, 42(5):1 096-1 112.
Gómez F, Nagahama Y, 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 Océanides, 27(1):65-140.
Gu H F, Luo Z H, Zhang X D, Fang Q. 2013. Morphology, ultrastructure and phylogeny of Takayama xiamenensis sp. nov. (Gymnodiniales, Dinophyceae) from the East China Sea. Phycologia, 52(3):256-265.
Gu H F. 2007. Resting cysts, life cycle and phylogenetic analysis of typical algae from southeastern China Sea.Ocean University of China, Qingdao, China. (in Chinese with English abstract)
Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3):234-236.
Hansen G, Daugbjerg N, Henriksen P. 2000. Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (=Gyrodinium aureolum) based on morphology, pigment composition, and molecular data.Journal of Phycology, 36(2):394-410.
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.
Henrichs D W, Sosik H M, Olson R J, Campbell L. 2011.Phylogenetic analysis of Brachidinium capitatum(Dinophyceae) from the Gulf of Mexico indicates membership in the Kareniaceae. Journal of Phycology, 47(2):366-374.
Hoagland P, Jin D, Polansky L Y, Kirkpatrick B, Kirkpatrick G, Fleming L E, Reich A, Watkins S M, Ullmann S G, Backer L C. 2009. The costs of respiratory illnesses arising from Florida Gulf Coast Karenia brevis blooms. Environmental Health Perspectives, 117(8):1 239-1 243.
Holland P T, Shi F, Satake M, Hamamoto Y, Ito E, Beuzenberg V, McNabb P, Munday R, Briggs L, Truman P, Gooneratne R, Edwards P, Pascal S W. 2012. Novel toxins produced by the dinoflagellate Karenia brevisulcata. Harmful Algae, 13(1):47-57.
Kempton J W, Lewitus A J, Deeds J R, Law J M, Place A R. 2002. Toxicity of Karlodinium micrum (Dinophyceae)associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae, 1(2):233-241.
Law P C, LEE Y K. 2013. Harmful Marine Microalgae in Hong Kong. Agriculture, Fisheries and Conservation Department. Hong Kong, China. p. 67-77.
Lin Y Y, Risk M, Ray S M, Van Engen D, Clardy J, Clardy J, James J C, Nakanishi K. 1981. Isolation and structure of brevetoxin B from the "red tide" dinoflagellate Ptychodiscus brevis (Gymnodinium breve). Journal of the American Chemical Society, 103(22):6 773-6 775.
Litaker R W, Vandersea M W, Kibler S R, Reece K S, Stokes N A, Steidinger K A, Millie D F, Bendis B J, Pigg R J, Tester P A. 2003. Identification of Pfiesteria piscicida(Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. Journal of Phycology, 39(4):754-761.
Liu R Y. 2008. Checklist of Marine Biota of China Seas.Science Press, Beijing, China. p.177. (in Chinese)
Miles C O, Wilkins A L, Stirling D J, MacKenzie A L. 2003.Gymnodimine C, an isomer of gymnodimine B, from Karenia selliformis. Journal of Agricultural and Food Chemistry, 51(16):4 838-4 840.
Mooney B D, Nichols P D, De Salas M F, Hallegraeff G M. 2007. Lipid, fatty acid, and sterol composition of eight species of Kareniaceae (Dinophyta):chemotaxonomy and putative lipid phycotoxins. Journal of Phycology, 43(1):101-111.
Naar J P, Flewelling L J, Lenzi A, Abbott J P, Granholm A, Jacocks H M, Gannon D, Henry M, Pierce R, Baden D G, Wolny J, Landsberg J H. 2007. Brevetoxins, like ciguatoxins, are potent ichthyotoxic neurotoxins that accumulate in fish. Toxicon, 50(5):707-723.
Nézan E, Siano R, Boulben S, Six C, Bilien G, Chèze K, Duval A, Le Panse S, Quéré J, Chomérat N. 2014. Genetic diversity of the harmful family Kareniaceae(Gymnodiniales, Dinophyceae) in France, with the description of Karlodinium gentienii sp. nov.:a new potentially toxic dinoflagellate. Harmful Algae, 40(40):75-91.
Nunn G B, Theisen B F, Christensen B, Arctander P. 1996.Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution, 42(2):211-223.
Omura T, Iwataki M, Borja V M, Takayama H, Fukuyo Y. 2012. Marine Phytoplankton of the Western Pacific.Kouseisha Kouseikaku Company, Tokyo, Japan. p.73.
Reñé A, Camp J, Garcés E. 2015. Diversity and phylogeny of Gymnodiniales (Dinophyceae) from the NW Mediterranean Sea revealed by a morphological and molecular approach. Protist, 166(2):234-263.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3:bayesian phylogenetic inference under mixed models.Bioinformatics, 19(12):1 572-1 574.
Satake M, Shoji M, Oshima Y, Naoki H, Fujita T, Yasumoto T. 2002. Gymnocin-A, a cytotoxic polyether from the notorious red tide dinoflagellate, Gymnodinium mikimotoi.Tetrahedron Letters, 43(33):5 829-5 832.
Satake M, Tanaka Y, Ishikura Y, Oshima Y, Naoki H, Yasumoto T. 2005. Gymnocin-B with the largest contiguous polyether rings from the red tide dinoflagellate, Karenia(formerly Gymnodinium) mikimotoi. Tetrahedron Letters, 46(20):3 537-3 540.
Scholin C A, Herzog M, Sogin M, Anderson D A. 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.
Scorzetti G, Brand L E, Hitchcock G L, Rein K S, Sinigalliano C D, Fell J W. 2009. Multiple simultaneous detection of Harmful Algal Blooms (HABs) through a high throughput bead array technology, with potential use in phytoplankton community analysis. Harmful Algae, 8(2):196-211.
Seki T, Satake M, Mackenzie L, Kaspar H F, Yasumoto T. 1995. Gymnodimine, a new marine toxin of unprecedented structure isolated from New Zealand oysters and the dinoflagellate, Gymnodinium sp. Tetrahedron Letters, 36(39):7 093-7 096.
Shimizu Y, Chou H N, Bando H, Van Duyne G, Clardy J. 1986.Structure of brevetoxin A (GB-1 toxin), the most potent toxin in the Florida red tide organism Gymnodinium breve(Ptychodiscus brevis). Journal of the American Chemical Society, 108(3):514-515.
Siano R, Kooistra W H C F, Montresor M, Zingone A. 2009.Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia, 48(1):44-65.
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.
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.
Tester P A, Turner J T, Shea D. 2000. Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. Journal of Plankton Research, 22(1):47-61.
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.
White T J, Bruns T D, Lee S B, Taylor J W. 1990. Amplification and direct sequencing of fungal ribosomal DNA for phylogenetics. In:Innis M A, Gelfand D H, Sninsky J J, White T J eds. PCR Protocols:A Guide to the Method and Applications. Academic Press, New York, USA. p.315-322.
Yang Z B, Hodgkiss I J, Hansen G. 2001. Karenia longicanalis sp. nov. (Dinophyceae):a new bloom-forming species isolated from Hong Kong, May 1998. Botanica Marina, 44(1):67-74.
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.
Zapata M, Rodríguez F, Garrido J L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton:a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series, 195(3):29-45.