Isolation of an algicide from a marine bacterium and its effects against the toxic dinoflagellate Alexandrium catenella and other harmful algal bloom species

Journal of Microbiology

Volumn 53, Issue 8, 2015, Pages 511-517

  Kim, Yun Sook ^a   Son, Hong Joo ^b   Jeong, Seong Yun ^c  

^a Marine Bioprocess Co Ltd   (South Korea)

^b Pusan National University   (South Korea)

^c Catholic University of Daegu   (South Korea)

Author keywords

1 acetyl carboline; Alexandrium catenella; algicidal activity; algicide; Brachybacterium; harmful algal bloom species

Indexed keywords

1-ACETYL-BETA-CARBOLINE; ANTIINFECTIVE AGENT; CARBOLINE DERIVATIVE; RNA 16S;

CHEMISTRY; DINOFLAGELLATE; DRUG EFFECTS; GENETICS; PHYLOGENY;

ANTI-BACTERIAL AGENTS; CARBOLINES; DINOFLAGELLIDA; PHYLOGENY; RNA, RIBOSOMAL, 16S;

EID: 84938404369     PISSN: 12258873     EISSN: 19763794     Source Type: Journal    
DOI: 10.1007/s12275-015-5303-1     Document Type: Article

References (48)

1. Ahn, C.Y., Joung, S.H., Jeon, J.W., Kim, H.S., Yoon, B.D., and Oh, H.M. 2003. Selective control of cyanobacteria by surfactin-containing culture broth of Bacillus subtilis C1. Biotechnol. Lett.25, 1137–1142.
2. Amaro, A.M., Fuentes, M.S., Ogalde, S.R., Venegas, J.A., and Suarez-Isla, B.A. 2005. Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J. Eukaryot. Microbiol.52, 191–200.
3. Anderson, D.M., Alpermann, T.J., Cembella, A.D., Collos, Y., Masseret, E., and Montresor, M. 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae14, 10–35.
4. Bravo, V.M., Maso, M., Figueroa, R.I., and Ramilo, I. 2008. Alexandrium catenella and Alexandrium minutum blooms in the Mediterranean Sea: toward the identification of ecological niches. Harmful Algae7, 515–522.
5. Doucette, G.J., McGovern, E.R., and Babinchak, J.A. 1999. Algicidal bacteria active against Gymnodinium breve (Dinophyceae). I. Bacterial isolation and characterization of killing activity. J. Phycol.35, 1447–1454.
6. Droop, M.R. 1967. A procedure for routine purification of algae cultures with antibiotics. Brit. Phycol. Bull.3, 295–297.
7. Fukami, K., Yuzawa, A., Nishijima, T., and Hata, Y. 1992. Isolation and properties of a bacterium inhibiting the growth of Gymnodinium nagasakiense. Nippon Suisan Gakkaishi58, 1073–1077.
8. Glibert, P.M., Anderson, D.M., Gentien, P., Graneli, E., and Sellner, K.G. 2005. The global complex phenomena of harmful algal blooms. Oceanography18, 136–147.
9. Guillard, R.R.L. and Ryther, J.H. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve). Gran. Can. J. Microbiol.8, 229–235.
10. Hold, G.L., Smith, E.A., Rappé, M.S., Maas, E.W., Moore, E.R.B., Stroempl, C., Stephen, J.R., Prosser, J.I., Birkbeck, T.H., and Gallacher, S. 2001. Characterisation of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella rochoidea. FEMS Microbiol. Ecol.37, 161–173.
11. Holmström, C. and Kjelleberg, S. 1999. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol. Ecol.30, 285–293.
12. Imai, I., Ishida, Y., and Hata, Y. 1993. Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan. Mar. Biol.116, 527–532.
13. Imai, I., Nagagiri, S., Nagai, K., Nagasaki, K., Itakura, S., and Yamaguchi, M. 1998. Fluctuations of algicidal microorganisms against the harmful dinoflagellate Heterocapsa circularisquama in Ago Bay, Mie Prefecture, Japan. Bull. Nansei Natl. Fish. Res. Inst.31, 53–61.
14. Imai, I., Sunahara, T., Nishikawa, T., Hori, Y., Kondo, R., and Hiroishi, S. 2001. Fluctuations of the red tide flagellates Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in the Seto Inland Sea, Japan. Mar. Biol.138, 1043–1049.
15. Jeong S.Y., Ishida, K., Ito, Y., Okada, S., and Murakami, M. 2003. Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. SY-1, against the harmful dinoflagellate, Cochlodinium polykrikoides. Tetrahedron Lett.44, 8005–8007.
16. Jeong, S.Y., Park, Y.T., and Lee, W.J. 2000. Isolation of marine bacteria killing red tide microalgae, III. Algicidal effects of marine bacterium, Micrococcus sp. LG-5 against the harmful dinoflagellate, Cochlodinium polykrikoides. J. Kor. Fish. Soc.33, 331–338.
17. Kim, H.G. 1997. Recent harmful algal blooms and mitigation strategies in Korea. Ocean Polar Res.19, 185–192.
18. Kim, D., Oda, T., Muramatsu, T., Kim, D., Matsuyama, Y., and Honjo, T. 2002. Possible factors responsible for the toxicity of Cochlodinium polykrikoides, a red tide phytoplankton. Comp. Biochem. Physiol. C-Toxicol. Pharmacol.132, 415–423.
19. Kim, M.C., Yoshinaga, I., Imai, I., Nagasaki, K., Itakura, S., and Ishida, Y. 1998. A close relationship between algicidal bacteria and termination of Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Mar. Ecol. Prog. Ser.170, 25–32.
20. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. J. Mol. Evol.16, 111–120.
21. Kodani, S., Imoto, A., Mitsutani, A., and Murakami, M. 2002. Isolation and identification of the antialgal compound, harmane (1-methyl-β-carboline), produced by the algicidal bacterium, Pseudomonas sp. K44-1. J. Appl. Phycol.14, 109–114.
22. Lee, D.S., Eom, S.H., Jeong, S.Y., Shin, H.J., Je, J.Y., Lee, E.W., Chung, Y.H., Kang, C.K., and Lee, M.S. 2013. Anti-methicillin-resistant Staphylococcus aureus (MRSA) substance from the marine bacterium Pseudomonas sp. UJ-6. Environ. Toxicol. Pharmacol.35, 171–177.
23. Lee, S.O., Kato, J., Nakashima, K., Kuroda, A., Ikeda, T., Takiguchi, N., and Ohtake, H. 2002. Cloning and characterization of extracellular metal protease gene of the algicidal marine bacterium Pseudoalteromonas sp. strain A28. Biosci. Biotechnol. Biochem.66, 1366–1369.
24. Lewin, R.A. 1997. Suprospira grandis: a flexibacterium that can catch bacterial prey by “ixotrophy.” Microb. Ecol.34, 232–236.
25. Lovejoy, C., Bowman, J.P., and Hallegraeff, G.M. 1998. Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl. Environ. Microbiol.64, 2806–2813.
26. MacFaddin, J.F. 1980. Biochemical tests for identification of medical bacteria, pp. 36–308, 2nd ed. Williams and Wilkins Co., Baltimore, USA.
27. Mayali, X. and Azam, F. 2004. Algicidal bacteria in the sea and their impact on algal blooms. J. Eukaryot. Microbiol.51, 139–144.
28. Mitsutani, A., Takesue, K., Kirita, M., and Ishida, Y. 1992. Lysis of Skeletonema costatum by Cytophaga sp. isolated from the coastal water of the Ariake Sea. Nippon Suisan Gakkaishi58, 2159–2167.
29. Mitsutani, A., Yamasaki, I., Kitaguchi, H., Kato, J., Ueno, S., and Ishida, Y. 2001. Analysis of algicidal proteins of a diatom-lytic marine bacterium Pseudoalteromonas sp. strain A25 by two-dimensional electrophoresis. Phycologia40, 286–291.
30. Nakashima, T., Miyazaki, Y., Matsuyama, Y., Muraoka, W., Yamaguchi, K., and Oda, T. 2006. Producing mechanism of an algicidal compound against red tide phytoplankton in a marine bacterium γ-proteobacterium. Appl. Microbiol. Biotechnol.73, 684–690.
31. Park, Y.T., Park, J.B., Chung, S.Y., Song, B.S., Lim, W.A., Kim, C.H., and Lee, W.J. 1998. Isolation and algicidal properties of Micrococcus sp. LG-1 possessing killing activity for harmful Dinoflagellate Cochlodinium polykrikoides. J. Kor. Fish. Soc.31, 767–773.
32. Proksa B., Uhrin D., Sturdikova M., and Fuska, J. 1990. 1-Acetyl-β-carboline, a new metabolite of Streptomyces kasugaensis. Act. Biotechnol.10, 337–340.
33. Rainey, F.A., Ward-Rainey, N., Kroppenstedt, R.M., and Stackebrandt, E. 1996. The genus Norcardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Norcardiopsaceae fam. nov. Int. J. Syst. Bacteriol.46, 1088–1092.
34. Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol.24, 189–204.
35. Sala, M.M., Balague, V., Pedros-Alio, C., Massana, R., Felipe, J., Arin, L., Illoul, H., and Estrada, M. 2005. Phylogenetic and functional diversity of bacterioplankton during Alexandrium spp. blooms. FEMS Microbiol. Ecol.54, 257–267.
36. Shirling, E.B. and Gottlieb, D. 1996. Methods for characterization of Streptomyces species. Int. J. Syst. Bacteriol.16, 313–340.
37. Skerratt, J.H., Bowman, J.P., Hallegraeff, G.M., James, S., and Nichols, P.D. 2002. Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Mar. Ecol. Prog. Ser.244, 1–15.
38. Su, J.Q., Yang, X.R., Zheng, T.L., Tian, Y., Jiao, N.Z., Cai, L.Z., and Hong, H.S. 2007. Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful Algae6, 799–810.
39. Su, J.Q., Yang, X.R., Zhou, Y.Y., and Zheng, T.L. 2011. Marine bacteria antagonistic to the harmful algal bloom species Alexandrium tamarense (Dinophyceae). Biol. Control56, 132–138.
40. Taga, N. 1968. Some ecological aspects of marine bacteria in the Kuroshio Current. Bull. Misaki Mar. Biol.12, 65–76.
41. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol.28, 2731–2739.
42. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.22, 4673–4680.
43. Wang, X., Gong, L., Liang, S., Han, X., Zhu, C., and Li, Y. 2005. Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae4, 433–443.
44. Wang, B., Yang, X., Lu, J., Zhou, Y., Su, J., Tian, Y., Zhang, J., Wang, G., and Zheng, T. 2012. A marine bacterium producing protein with algicidal activity against Alexandrium tamarense. Harmful Algae13, 83–88.
45. Whyte, J.N.C., Haigh, N., Ginther, N.G., and Keddy, L.J. 2001. First record of blooms of Cochlodinium sp. (Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycologia40, 298–304.
46. Yang, X., Li, X., Zhou, Y., Zheng, W., Yu, C., and Zheng, T. 2014. Novel insights into the algicidal bacterium DH77-1 killing the toxic dinoflagellate Alexandrium tamarense. Sci. Total Environ.482–483, 116–124.
47. Yoshinaga, I., Kawai, T., and Ishida, Y. 1997. Analysis of algicidal ranges of the bacterial killing the marine dinoflagellate Gymnodinium mikimotoi isolated from Tanabe Bay, Wakayama Pref., Japan. Fish. Sci.61, 780–786.
48. Yoshinaga, I., Kawai, T., Takeuchi, T., and Ishida, Y. 1995. Distribution and fluctuation of bacteria inhibiting the growth of a marine red tide phytoplankton Gymnodinium mikimotoi in Tanabe Bay (Wakayama Pref., Japan). Fish. Sci.61, 780–786.