Browse > Article
http://dx.doi.org/10.7850/jkso.2016.21.4.158

Species Diversity of the Dinoflagellate Genus Alexandrium in the Coastal Waters of Korea during Summer 2013  

KIM, JAE SEONG (Water&Eco-Bio Corporation)
PARK, KYUNG WOO (Climate Change Research Division, National Institute of Fisheries Sciences)
YOUN, SEOK HYUN (Climate Change Research Division, National Institute of Fisheries Sciences)
LIM, WEOL AE (Climate Change Research Division, National Institute of Fisheries Sciences)
YOO, YEONG DU (Department of Marine Biotechnology, College of Ocean Science and Technology, Kunsan National University)
SEONG, KEYONG AH (Department of Marine Biotechnology, College of Ocean Science and Technology, Kunsan National University)
YIH, WON HO (Department of Marine Biotechnology, College of Ocean Science and Technology, Kunsan National University)
Publication Information
The Sea:JOURNAL OF THE KOREAN SOCIETY OF OCEANOGRAPHY / v.21, no.4, 2016 , pp. 158-170 More about this Journal
Abstract
We investigated the occurrence of the dinoflagellate genus Alexandrium in the nineteen Korean coastal sites from July to October 2013. Alexandrium-like planktonic cells were microscopically observed only in four out of the 19 sampling sites. From the samples containing Alexandrium-like cells 22 clonal cultures of Alexandrium species were established by single cell or single chain isolation method. Taxonomic identity of the 4 different strains ascertained by the robust analyses of morphological and molecular genetic characteristics were confirmed to be A. catenella, A. affine, A. fraterculus and an unidentified Alexandrium sp. for which strain WEB-Alex-01 was assigned. It was ascertained that in spite of hot summer diverse Alexandrium species attaining up to four were distributed in the study area, in contrast with the long empirical recognition that the emergence of Alexandrium species is restricted to cooler seasons like spring or autumn in Korean coastal waters. Morphology and genetic characteristics of Alexandrium sp. strain WEB-Alex-01 are different from any other previously reported Alexandrium species from Korean seas, which implies that further studies on taxonomic, physiological, ecological and toxicological properties of the newly recorded Alexandrium species are needed.
Keywords
Alexandrium; Species Diversity; A. catenella; A. affine; A. fraterculus; Taxonomy;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Bolch, C.J.S. and M.F. Salas, 2007. A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium "tamarensis complex" to Australasia. Harmful Algae, 6: 465-485.   DOI
2 Bricelj, V.M. and S.E. Shumway, 1998. Paralytic shellfish toxins in bivalve molluscs: Occurrence, transfer kinetics, and biotransformation. Rev. Fish. Sci., 6: 315-383.   DOI
3 Chang, D.S., I.S. Shin, J.H. Pyeun and Y.H. Park, 1987. A study on paralytic shellfish poision of sea mussel, Mytilus edulis : Food poisoning accident in Gamchun Bay, Pusan, Korea, 1986. Bull. Korean Fish. Soc., 20: 293-299 (in Korean).
4 Cho, C.H., 1978. On the Gonyaulax red tide in Jinhae Bay. Bull. Korean Fish. Soc. 11: 111-114 (in Korean).
5 Dlegado, M., M. Estrada, J. Camp, J. Fernandez, M. Santmarti and C. Lieti, 1990. Development of a toxic Alexandrium minutum Halim (Dinophyceae) bloom in the harbour of Sant Carles de la Rapita (Ebro Delta, northwestern Mediterranean). Scient. Mar., 54: 1-7.
6 ECOHAB, 1995. The ecology and oceanography of harmful algal blooms. A national research agenda. Woods Hole Oceanographic Institute, Woods Hole, MA, 66 pp.
7 Fraga, S., N. Sampedro, J. Larsen, O. Moestrup and A.J. Calado, 2015. Arguments against the proposal 2302 by John & al. to reject the name Gonyaulax catenella (Alexandrium catenella). Taxon, 64(3): 634-635.   DOI
8 Fritz, L. and R.E. Triemer, 1985. A rapid simple technique utilizing calcofluor white M2R for the visualization of dinoflagellate thecal plates. J. Phycol., 21: 662-664.
9 McCauley, L.A.R., D.L. Erdner, S. Nagai, M.L. Richlen and D.M. Anderson, 2009. Biogeographic analysis of the globally distributed harmful algal bloom species Alexandrium minutum (dinophyceae) based on rRNA gene sequences and microsatellite markers. J. Phycol., 45: 454-463.   DOI
10 Lim, W-A., S.Y. Kim, M.K. Bae, S.Y. Park, Y.H. Chen and I.K. Chung, 2011. Distribution of Alexandrium spp. and marine environmental change. Korea Marine Science and Technology Council Joint Conference Proceeding. 260 pp.
11 Medlin, L., H.J. Elwood, S. Stickel and M.L. Sogin, 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene., 71: 491-499.   DOI
12 Menden-Deuer, S., E.J. Lessard, J. Satterberg and D. Grunbaum, 2005. Growth rates and starvation survival of three species of the pallium feeding, thecate dinoflagellate genus Protoperidinium. Aquat. Microb. Ecol., 41: 145-152.   DOI
13 Montresor, M., 1995. The life history of Alexandrium pseudogonyaulax(Gonyaulacales, Dinophyceae). Phycologia, 34: 444-448.   DOI
14 Nagai, S., M. Yukihiro, S.H. Oh and S. Itakura, 2004. Effects of nutrients and temperature on encystment of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) isolated from Hiroshima Bay, Japan. Plankton Biology & Ecology, 51: 103-109.
15 Halim, Y., 1960. Alexandrium minutum nov. g. nov. sp. dinoflagelle provocant des 'eaux rouges'. Vie Milieu, 11: 102-105.
16 Fukuyo, Y., K. Yoshida and H. Inoue, 1985. Protogonyaulax in Japanese costal waters. In: Toxic Dinoflagellates, edited by Anderson, D.M., A.W. White and D.G. Baden, Elsevier, Amsterdam, pp. 27-32.
17 Giacobbe, M.G., F.D. Oliva and G. Maimone, 1996. Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP potential producer, in a Mediterranean lagoon. Estuar. Coast. Shelf Sci., 42: 539-549.   DOI
18 Glibert, P.M., J.M. Burkholder, T.M. Kana, J. Alexander, H. Skelton and C. Shilling, 2009. Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquat. Microb. Ecol., 55: 17-30.   DOI
19 Nguyen-Ngoc, L., 2004. An autecological study of the potentially toxic dinoflagellate Alexandrium affine isolated from Vietnamese waters. Harmful Algae, 3: 117-129.   DOI
20 Nygaard, K. and A. Tobiesen, 1993. Bacterivory in algae: a survival strategy during nutrient limitation. Limnol. Oceanogr., 38: 273-279.   DOI
21 Hallegraeff, G.M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, 32: 79-99.   DOI
22 Han, M.S., J.K. Jeon and Y.H. Yoon, 1993. Distribution and toxin profiles of Alexandrium tamarense (Lebour) Balech (Dinoflagellate) in the Southeastern coastal waters, Korea. Korean J. Phycol., 8: 7-13.
23 Huelsenbeck, J.P. and F. Ronquist, 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17: 754-755.   DOI
24 Jacobson, D.M. and D.M. Anderson, 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol., 32: 279-285.   DOI
25 Park, T.K., W.A. Lim, Y.T. Park, C.K. Lee and H.J. Jeong, 2013. Economic impact, management and mitigation of red tides in Korea. Harmful Algae, 30S: S131-S143.
26 Oh, S.J., J.A. Park, H.K. Kwon, H.S. Yang and W.A. Lim, 2012. Ecophysiological studies on the population dynamics of two toxic dinoflagellates Alexandrium tamarense and Alexandrium catenella isolated from the southern coast of Korea I. Effects of temperature and salinity in the growth. J. Korean Soc. Mar. Environ. Engine., 15: 133-144 (in Korean).   DOI
27 Park, J.K., 2008. Development of paralytic shellfish poisoning toxification and detection of the genus Alexandrium by using rea-time PCR assay in Jinhae Bay, Korea. Ph.D. Thesis, Pukyong National University, Busan, 47 pp (in Korean).
28 Park, T.K. and Y.S. Kang, 2009. Temporal changes in abundances of the toxic dinoflagellate Alexandrium minutum (Dinophyceae) in Chinhae Bay, Korea. J. Environ. Sciences, 18: 1331-1338.   DOI
29 Paulsen, O., 1904. Plankton investigation in the waters round Iceland in 1903. Medd. Komm. Havunders. Kopenhaven, Ser. Plankton, 1: 1-40.
30 Reimann, B.E.F., E.L. Duke and G.L. Floyd, 1980. Fixation, embedding, sectioning and staining of algae for election microscopy. p. 285-303, In: Handbook of Phycological Methods. ed. by G. Elisabeth. Cambridge Univ. Press, London.
31 Ronquist, F. and J.P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572-17574.   DOI
32 Jeong, H.J., Y.D. Yoo, K.A. Seong, J.H. Kim, J.Y. Park, S.H. Kim, S.H. Lee, J.H. Ha and W.H. Yih, 2005c. Feeding by the mixotrophic dinoflagellate Gonyaulax polygramma: mechanisms, prey species, the effects of prey concentration, and grazing impact. Aquat. Microb. Ecol., 38: 249-257.   DOI
33 Jeong, H.J., J.H. Shim, J.S. Kim, J.Y. Park, C.W. Lee and Y. Lee, 1999. The feeding by the thecate mixotrophic dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser., 176: 263-277.   DOI
34 Jeong, H.J., Y.D. Yoo, J.Y. Park, J.Y. Song, S.T. Kim, S.H. Lee, K.Y. Kim and W.H. Yih, 2005a. Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species preciously known to be mixotrophic. Aquat. Microb. Ecol., 40: 133-150.   DOI
35 Jeong, H.J., J.Y. Park, J.H. Nho, M.O. Park, J.H. Ha, K.A. Seong, J. Chang, C.N. Seong, K.Y. Lee and W.H. Yih, 2005b. Feeding by the red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol., 41: 131-143.   DOI
36 Seong, K.A., H.J. Jeong, S. Kim, G.H. Kim and J.H. Kang, 2006. Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marine bacteria in the Korean waters. Mar. Ecol. Prog. Ser., 322: 85-97.   DOI
37 Jeong, H.J., Y.D. Yoo, K.H. Lee, T.H. Kim, K.A. Seong, N.S. Kang, S.Y. Lee, J.S. Kim, S. Kim and W.H. Yih, 2013. Red tides in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tide organisms and environmental factors. Harmful Algae, 30S: S75-S88.
38 John, U., R.W. Litaker, M. Montresor, S. Murray, M.L. Brosnahan and D.M. Anderson, 2014a. Formal Revision of the Alexandrium tamarense Species Complex (Dinophyceae) Taxonomy: The Introduction of Five Species with Emphasis on Molecular-based (rDNA) Classification. Protist., 165: 779-804.   DOI
39 John, U., W. Litaker, M. Montresor, S. Murray, M.L. Brosnahan and D.M. Anderson, 2014b. (2302) Proposal to reject the name Gonyaulax catenella (Alexandrium catenella) (Dinophyceae). Taxon, 63(4): 932-933.   DOI
40 Scholin, C.A., M. Herzog, M. Sogin and D.M. Anderson, 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
41 Shin, H.H., J.S. Park Y.O. Kim, S.H. Baek, D. Lim and Y.H. Yoon, 2012. Dinoflagellate cyst production and flux in Gamak Bay, Korea: A sediment trap study. Mar. Micropaleontol., 94-95: 72-79.   DOI
42 Shin, H.H., K. Mizushima, S.J. Oh, J.S. Park, I.H. Noh, M. Iwataki, K. Matsuoka and Y.H. Yoon, 2010. Reconstruction of historical nutrient levels in Korean and Japanese coastal areas based on dinoflagellate cyst assemblages. Mar. Poll. Bull., 60: 1243-1258.   DOI
43 Shin, H.H., S.H. Baek, Z. Li, M.S. Han, S.J Oh, S.H. Youn, Y.S. Kim, D.K. Kim and W.A. Lim, 2014. Resting cysts, and effects of temperature and salinity on the growth of vegetative cells of the potentially harmful species Alexandrium insuetum Balech (Dinophyceae). Harmful Algae, 39: 175-184.   DOI
44 Stamatakis, A., 2006. Phylogenetic models of rate heterogeneity: a high performance computing perspective. Proceedings 20th IEEE International Parallel & Distributed Processing Symposium, Rhodes Island, 8 pp.
45 Stoecker, D.K. and N.K. Sanders, 1985. Differential grazing by Acartia tonsa on a dinoflagellate and a tintinnid. J. Plankton. Res., 7: 85-100.   DOI
46 Stoecker, D.K., A. Li, D.W. Coats, D.E. Gustafson and M.K. Nannen, 1997. Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser., 152: 1-12.   DOI
47 Kim, H-G., J.S. Kim and S.G. Lee, 1990. Coastal algal blooms caused by the cyst-forming Dinoflagellates. Bull. Korean Fish. Soc., 23: 468-474.
48 Kamiyama, T. and Y. Matsuyama, 2005. Temporal changes in the ciliate assemblage and consecutive estimates of their grazing effect during the course of a Heterocapsa circularisquama bloom. J. Plankton. Res., 27: 303-311.   DOI
49 Kao, C.Y., 1993. Paralytic Shellfish Poisoning. In: Algal Toxins in Seafood and Drinking Water, edited by Falconer, I.R, Academic Press, London, pp. 75-86.
50 Kim, C.H., 1994. Germinability of resting cysts associated with occurrence of toxic dinoflagellate Alexandrium species. J. Aquaculture, 7: 251-264 (in Korean).
51 Kim, K.Y., M. Yoshida, Y. Fukuyo and C.H. Kim, 2002. Morphological Observation of Alexandrium tamarense (Lebour) Balech, A. catenella (Whedon et Kofoid) Balech and One Related Morphotype (Dinophyceae) in Korea. Algae, 17: 11-19.   DOI
52 Taylor, F.J.R., Y. Fukuyo and J. Larsen, 1995. Taxonomy of harmful dinoflagellates. In: Manual on Harmful Marine Micro Algae, edited by Hallegaeff, G.M., D.M. Anderson and A.D. Cembella, IOC Manuals and Guides No.33. Intergovernmental Oceanographic Commission of UNESCO, Paris, 33 pp.
53 Kim, S.J., 2006. Patterns in host range two strains of Amoebophrya (Dinophyta) infecting thecate dinoflagellates: Amoebophyra spp. ex Alexandrium affine and Gonyaulax polygramma. J. Phycol., 42: 1170-1173.   DOI
54 Kim, S.J., M.G. Park, W.H. Yih and D.W. Coats, 2004. Infection of the bloom-forming thecate dinoflagellates Alexandrium affine and Gonyaulax spinifera by two strains of Amoebophrya (Dinophyta). J. Phycol., 40: 815-822.   DOI
55 Larkin, M.A., G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson and D.G. Higgins, 2007. Clustal w and clustal $\times$ version 2.0. Bioinformatics, 23: 2947-2948.   DOI
56 Swofford, D.L., 2002. PAUP* 4.0: Phylogenetic analysis using parsimony, version 10. Computer program distributed by Sinauer Associates, Sunderland, MA.
57 Tamura, K., J. Dudley, M. Nei and S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software v. 4.0. Mol. Biol. Evol., 24: 1596-1599.   DOI
58 Townsend, D.W., N.R. Pettigrew and A.C. Thomas, 2001. Offshore blooms of the red tide dinoflagellate, Alexandrium sp. in the Gulf of Maine. Continental Shelf Res. 21: 347-369.   DOI
59 Wang, D.Z., S.G. Zhang, H.F. Gu, L.L. Chan and H.S. Hong, 2006. Paralytic shellfish toxin profiles and toxin variability of the genus Alexandrium (Dinophyceae) isolated from the Southeast China Sea. Toxicon, 48: 138-151.   DOI
60 Wyatt, T. and I.R. Jenkinson, 1997. Notes on Alexandrium population dynamics. J. Plank. Res., 19: 551-575.   DOI
61 Yoo, Y.D., H.J Jeong, M.S. Kim, N.S. Kang, J.Y. Song, W.G. Shin, K.Y. Kim and K.T. Lee, 2009. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonama costatum. J. Eukaryot. Microbiol., 56: 413-420.   DOI
62 Lee, J.S., I.S. Shin, Y.M. Kim and D.S. Chang, 1997. Paralytic shellfish toxins in the mussel, Mytilus edulis, caused the shellfish poisoning accident at Geoje, Korea, in 1996. J. Korean Fish. Soc., 30: 158-160 (in Korean).
63 Lee, S.W., H.W. Lee, J.G. Park, J.A. Lee and Y.S. Park, 1998. Molecular phylogeny of phytoplankton isolated from red tides in southern coast of Korea. J. Korean Soc. Oceanogr., 3(2): 90-93 (in Korean).
64 Lee, H.O., K.H. Choi and M.S. Han, 2003. Spring bloom of Alexandrium tamarense in Chinhae Bay, Korea. Aqua. Microb. Ecol., 33: 271-278.   DOI
65 Lee, J.B., D.Y. Kim and J.A. Lee, 1998. Community Dynamics and Distribution of Dinoflagellates and Their Cysts in Masan-Chinhae Bay, Korea. J. Fish. Sci. Tech., 1: 283-292.
66 Li, A., D.K. Stoecker and D.W. Coats, 2000. Mixotrophy in Gyrodinium galatheanum (Dinophyceae): grazing responses to light intensity and inorganic nutrients. J. Phycol., 36: 33-45.
67 Lilly, E.L., K.M. Halanych and D.M. Anderson, 2005. Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae, 4: 1004-1020.   DOI
68 Anderson, D.M., D.M. Kulis, G.J. Doucette, J.C. Gallagher and E.T. Balech, 1994. Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada. Mar. Biol., 120: 467-478.   DOI
69 Anderson, D.M., 1997. Bloom dynamics of toxic Alexandrium species in the northeastern U.S.. Limnol. Oceanogr., 42: 1009-1022.   DOI
70 Anderson, D.M., 2009. Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean & Coastal Management, 52: 342-347.   DOI
71 Anderson, D.M., T.A. Alpermann, A.D. Cembella, Y. Collos, E. Masseret and M. Montresor, 2012. The globally distributed genus Alexandrium, Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae, 12: 10-35.
72 Balech, E., 1995. The genus Alexandrium Halim. Sherkin Island Marine Station, Cork, Ireland, 151 pp.
73 Berge, T., P.J. Hansen and O. Moestrup, 2008. Prey size spectrum and bioenergetics of the mixotrophic dinoflagellate Karlodinium armiger. Aquat. Microb. Ecol., 50: 289-299.   DOI
74 Bockstahler, K.R. and D.W. Coats, 1993. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J. Eukaryot. Microbiol., 40: 49-60.   DOI
75 Lim, P.T. and T. Ogata, 2005. Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae), Toxicon, 45: 699-710.   DOI
76 Lilly, E.L., K.M. Halanych and D.M. Anderson, 2007. Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol., 43: 1329-1338.   DOI
77 Lim, A.S., H.J. Jeong, J.H. Kim and S.Y. Lee, 2015. Description of the new phototrophic dinoflagellate Alexandrium pohangense sp. nov. from Korean coastal waters. Harmful Algae, 46: 49-61.   DOI