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http://dx.doi.org/10.4490/algae.2013.28.3.213

Morphology and molecular characterization of the epiphytic dinoflagellate Amphidinium massartii, isolated from the temperate waters off Jeju Island, Korea  

Lee, Kyung Ha (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Park, Kila (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Kang, Nam Seon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Yoo, Yeong Du (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Lee, Moo Joon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Lee, Jin-Woo (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Lee, Soojin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Kim, Taekyung (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University)
Kim, Hyung Seop (Department of Marine Biotechnology, College of Ocean Sciences, Kunsan National University)
Noh, Jae Hoon (Marine Resources Research Department, KIOST)
Publication Information
ALGAE / v.28, no.3, 2013 , pp. 213-231 More about this Journal
Abstract
Amphidinium massartii Biecheler is an epiphytic and toxic dinoflagellate. Prior to the present study, A. massartii has been reported in the waters off the Mediterranean, Australian, USA, and Canadian coasts. We isolated Amphidinium cells from the coastal waters of Jeju Island, Korea and their morphology and rDNA sequences indicated that they were A. massartii. Herein, we report for the first time the occurrence of A. massartii in the waters of the temperate region in the northwestern Pacific Ocean. The large subunit (LSU) rDNA sequences of the Korean strains were 0.7% different from those of an Australian strain of A. massartii CS-259, the closest species, but were 4.1-5.8% different from those of the other Australian strains and the USA strains of A. massartii and from those of Amphidinium sp. HG115 that was isolated from subtropical Okinawan waters. In phylogenetic trees based on LSU, internal transcribed spacer, small subunit rDNA, and cytochrome b sequences, the Korean strains belonged to the A. massartii clade, which was clearly divergent from the A. carterae clade. The morphology of the Korean A. massartii strains was similar to that of the originally described French strain and recently described Australian strain. However, we report for the first time here that scales were observed on the surface of the flagella. In conclusion, the Korean A. massartii strains have unique rDNA sequences, even though they have a very similar morphology to that of previously reported strains. This report extends the known range of this dinoflagellate to the temperate waters of the northwestern Pacific Ocean.
Keywords
Amphidinium carterae; Amphidinium massartii; epiphytic dinoflagellate; molecular analysis; phylogenetic analysis;
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1 Smith, S. W., Overbeek, R., Woese, C. R., Gilbert, W. & Gillevet, P. M. 1994. The genetic data environment an expandable GIU for multiple sequence analysis. Comput. Appl. Biosci. 10:671-675.
2 Stamatakis, A. 2006. RaxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.   DOI   ScienceOn
3 Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.   DOI   ScienceOn
4 Tamura, M., Takano, T. & Horiguchi, T. 2009. Discovery of a novel type of body scale in the marine dinoflagellate, Amphidinium cupulatisquama sp. nov. (Dinophyceae). Phycol. Res. 57:304-312.   DOI   ScienceOn
5 Taylor, D. L. 1971. On the symbiosis between Amphidinium klebsii (Dinophyceae) and Amphiscolops langerhansi (Turbellaria: Acoela). J. Mar. Biol. Assoc. U. K. 51:301- 313.   DOI
6 Watanabe, M. M., Suda, S. Inouye, I., Sawaguchi, T. & Chihara, M. 1990. Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll A- and B-containing endosymbiont. J. Phycol. 26:741-751.   DOI
7 Weekers, P. H. H., Gast, R. J., Fuerst, P. A. & Byers, T. J. 1994. Sequence variations in small-subunit ribosomal RNAs of Hartmannella vermiformis and their phylogenetic implications. Mol. Biol. Evol. 11:684-690.
8 Yasumoto, T. 1990. Marine microorganism toxins: an overview. In Graneli, E., Sundstrom, B., Edler, L. & Anderson, D. M. (Eds.) Toxic Marine Phytoplankton. Elsevier Science Publications, New York, pp. 3-8.
9 Zapata, M., Rodriquez, 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. Mar. Ecol. Prog. Ser. 195:29-45.   DOI
10 Zhang, H., Bhattacharya, D. & Lin, S. 2007. A three-gene dinoflagellate phylogeny suggests monophyly of Prorocentrales and a basal position for Amphidinum and Heterocapsa. J. Mol. Evol. 65:463-474.   DOI
11 Murray, S., Jorgensen, M. F., Daugbjerg, N. & Rhodes, L. 2004. Amphidinium revisited. II. Resolving species boundaries in the Amphidinium operculatum species complex (Dinophyceae), including the descriptions of Amphidinium trulla sp. nov. and Amphidinium gibbosum. comb. nov. J. Phycol. 40:366-382.   DOI   ScienceOn
12 Murray, S. & Patterson, D. J. 2002. The benthic dinoflagellate genus Amphidinium in south-eastern Australian waters, including three new species. Eur. J. Phycol. 37:279-298.   DOI   ScienceOn
13 Murray, S. A., Wiese, M., Stuken, A., Brett, S., Kellmann, R., Hallegraeff, G. & Neilan, B. A. 2011. sxtA-based quantitative molecular assay to identify saxitoxin-producing harmful algal blooms in marine waters. Appl. Environ. Microbiol. 77:7050-7057.   DOI   ScienceOn
14 Nayak, B. B., Karunasagar, I. & Karanasagar, I. 1997. Influence of bacteria on growth and hemolysin production by the marine dinoflagellate Amphidinium carterae. Mar. Biol. 130:35-39.   DOI
15 Pennick, N. C. & Clarke, K. J. 1977. The occurrence of scales in the peridinian dinoflagellate Heterocapsa triquetra (Ehrenb.) Stein. Br. Phycol. J. 12:63-66.   DOI
16 Ridgway, K. R. & Godfrey, J. S. 1997. Seasonal cycle of the East Australian Current. J. Geophys. Res. 102:22921-22936.   DOI
17 Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.   DOI   ScienceOn
18 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. J. Phycol. 30:999-1011.   DOI   ScienceOn
19 Sekida, S., Okuda, K., Katsumata, K. & Horiguchi, T. 2003. A novel type of body scale found in two strains of Amphidinium species (Dinophyceae). Phycologia 42:661-666.   DOI
20 Selina, M. S. & 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.   DOI
21 Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. & Higgins, D. G. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23:2947-2948.   DOI   ScienceOn
22 Larsen, J. 1985. Algal studies of the Danish Wadden Sea. II. A taxonomic study of psammobious dinoflagellates. Opera Bot. 79:14-37.
23 Larsen, J. 1988. An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27:366-377.   DOI
24 Larsen, J. & Patterson, D. J. 1990. Some flagellates (Protista) from tropical marine sediments. J. Nat. Hist. 24:801-937.   DOI   ScienceOn
25 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. J. Phycol. 39:754-761.   DOI   ScienceOn
26 Lopes, R. M. & Silveira, M. 1994. Symbiosis between a pelagic flatworm and a dinoflagellate from a tropical area: structural observations. Hydrobiologia 287:277-284.   DOI
27 Medlin, L., Elwood, H. J., Stickel, S. & Sogin, M. L. 1988. The characterization of enzymatically amplified eukaryokic 16S-like rRNA-coding regions. Gene 71:491-499.   DOI   ScienceOn
28 Monroe, E. A. & Van Dolah, F. M. 2008. The toxic dinoflagellate Karenia brevis encodes novel type I-like polyketide synthases containing discrete catalytic domains. Protist 159:471-482.   DOI   ScienceOn
29 Murray, S. A., Garby, T., Hoppenrath, M. & Neilan, B. A. 2012. Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata). PLoS ONE 7:e38253.   DOI
30 Morrill, L. C. & Loeblich, A. R. 3rd. 1981. A survey for body scales in dinoflagellates and a revision of Cachonina and Heterocapsa (Pyrrhophyta). J. Plankton Res. 3:53-65.   DOI
31 Horiguchi, T. 1997. Heterocapsa arctica sp. nov. (Peridiniales, Dinophyceae), a new marine dinoflagellate from the artic. Phycologia 36:488-491.   DOI
32 Huelsenbeck, J. P. & Ronquist, F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.   DOI   ScienceOn
33 Hulburt, E. M. 1957. The taxonomy of unarmored Dinophyceae of shallow embayments on Cape Cod, Massachusetts. Biol. Bull. 112:196-219.   DOI   ScienceOn
34 Ichikawa, H. & Beardsley, R. C. 2002. The current system in the Yellow and East China Sea. J. Oceanogr. 58:77-92.   DOI   ScienceOn
35 Iwataki, M., Hansen, G., Sawaguchi, T., Hiroishi, S. & Fukuyo, Y. 2004. Investigations of body scales in twelve Heterocapsa species (Peridiniales, Dinophyceae), including a new species H. pseudotriquetra sp. nov. Phycologia 43:394-403.   DOI
36 Jeong, H. J., Kang, H., Shim, J. S., Park, J. K., Kim, J. S., Song, J. Y. & Choi, H. J. 2001. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. Mar. Ecol. Prog. Ser. 218:77-86.   DOI
37 Jorgensen, M. F., Murray, S. & Daugbjerg, N. 2004. Amphidinium revisited. I. Redefinition of Amphidnium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. J. Phycol. 40:351-365.   DOI   ScienceOn
38 Coles, R. G., Lee Long, W. J., Watson, R. A. & Derbyshire, K. J. 1993. Distribution of seagrasses, and their fish and penaeid prawn communities, in Cairns Harbour, a tropical estuary, Northern Queensland, Australia. Aust. J. Mar. Freshw. Res. 44:193-210.
39 Kang, N. S., Jeong, H. J., Moestrup, O. & Park, T. G. 2011. Gyrodiniellum shiwhaense n. gen., n. sp., a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 58:284-309.   DOI   ScienceOn
40 Kang, N. S., Jeong, H. J., Moestrup, O., Shin, W., Nam, S. W., Park, J. Y., de Salas, M. F., Kim, K. W. & Noh, J. H. 2010. Description of a new planktonic mixotrophic dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from the coastal waters off western Korea: morphology, pigments, and ribosomal DNA gene sequence. J. Eukaryot. Microbiol. 57:121-144.   DOI   ScienceOn
41 Daugbjerg, N., Hansen, G., Larsen, J. & Moestrup, O. 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 39:302-317.   DOI   ScienceOn
42 Dodge, J. D. 1982. Marine dinoflagellates of the British Isles. Her Majesty's Stationary Office, London, 303 pp.
43 Dolapsakis, N. P. & Economou-Amilli, A. 2009. A new marine species of Amphidinium (Dinophyceae) from Thermaikos Gulf, Greece. Acta Protazool. 48:153-170.
44 Giovannoni, S. J., DeLong, E. F., Olsen, G. J. & Pace, N. R. 1988. Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J. Bacteriol. 170:720-726.   DOI
45 Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.   DOI
46 Horiguchi, T. 1995. Heterocapsa circularisquama sp. nov. (Peridiniales, Dinoiphyceae): a new marine dinoflagellate causing mass mortality of bivalves in Japan. Phycol. Res. 43:129-136.   DOI
47 Hallegraeff, G. M., McCausland, M. A. & Brown, R. K. 1995. Early warning of toxic dinoflagellate blooms of Gymnodinium catenatum in southern Tasmanian waters. J. Plankton Res. 17:1163-1176.   DOI   ScienceOn
48 Hansen, G. 1995. Analysis of the thecal pattern in the dinoflagellate Heterocapsa rotundata (Lohmann) comb. nov. (=Katodinium rotundatum (Lohmann) Loeblich). Phycologia 34:166-170.   DOI
49 Holdich, D. M. & Harrison, K. 1981. The sphaeromatid isopod genus Sphaeromopsis Holdich & Jones in African, Australian and South American waters. Crustaceana 41:286-300.   DOI
50 Baig, H. S., Saifullah, S. M. & Dar, A. 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae 5:133-140.   DOI   ScienceOn
51 Baillie, K. D. 1971. A taxonomic and ecological study of the intertidal, sand-dwelling dinoflagellates of the north Eastern Pacific Ocean. M.Sc. thesis, Department of Botany, University of British Columbia, Vancouver, BC, Canada, 110 pp.
52 Biecheler, B. 1952. Recherches sur les Peridiniens. Bull. Biol. France Belg. 36:1-149.
53 Calado, A. J., Craveiro, S. C. & Moestrup, O. 1998. Taxonomy and ultrastructure of a freshwater, heterotrophic Amphidinium (Dinophyceae) that feeds on unicellular protists. J. Phycol. 34:536-554.   DOI   ScienceOn
54 Clarke, K. J. & Pennick, N. C. 1972. Flagellar scales in Oxyrrhis marina Dujardin. Br. Phycol. J. 7:357-360.   DOI   ScienceOn
55 Clarke, K. J. & Pennick, N. C. 1976. The occurrence of body scales in Oxyrrhis marina Dujardin. Br. Phycol. J. 11:345-348.   DOI   ScienceOn