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Producing mechanism of an algicidal compound against red tide phytoplankton in a marine bacterium γ-proteobacterium

  • Applied Microbial and Cell Physiology
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Abstract

Strain MS-02-063, γ-proteobacterium, isolated from a coast area of Nagasaki, Japan, produced a red pigment which belongs to prodigiosin members. This pigment, PG-L-1, showed potent algicidal activity against various red tide phytoplanktons in a concentration-dependent manner. An understanding of a mechanism of PG-L-1 production by this marine bacterium may yield important new insights and strategies for preventing blooms of harmful flagellate algae in natural marine environments. Therefore, we analyzed the mechanisms of PG-L-1 production. In our previous study, the pigment production by this marine bacterium was completely inhibited at 1.56 μg/ml of erythromycin or 3.13 μg/ml of chloramphenicol, while minimal inhibitory concentrations for cell growth of erythromycin and chloramphenicol against this bacterium were >100 and 25 μg/ml, respectively. It is interesting to note that the ability of the pigment production in erythromycin-treated bacterium recovered by an addition of homoserine lactone. In fact, the pigment production was inhibited by β-cyclodextrin that inhibits autoinducer activities by a complex with N-acyl homoserine lactones. N-acyl homoserine lactones with autoinducer activities are ubiquitous bacterial signaling molecules that regulate gene expression in a cell density dependent process known as quorum sensing. Therefore, it was suggested that PG-L-1 produced by strain MS-02-063 is controlled by the homoserine lactone quorum sensing. It is speculated that this quorum sensing is involved in the production of algicidal agents of other marine bacteria. This bacterium and other algicidal bacteria might be concerned in regulating the blooms of harmful flagellate algae through the quorum sensing system.

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Abbreviations

N-AHL:

N-acyl homoserine lactones

DAPI:

4,6-Diamidino 2-phenylindole dihydrochloride

ESM:

Erd–Schreiber modified

HABs:

Harmful algal blooms

HPLC:

High performance liquid chromatography

MIC:

Minimal inhibitory concentration

YPG medium:

Yeast extract-peptone-glucose medium

References

  • Anderson DM (1997) Turning back the harmful red tide. Nature 388:513–514

    Article  CAS  Google Scholar 

  • Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signaling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786

    Article  CAS  Google Scholar 

  • Chang H, Richardson K, Uddstrom M, Pinkerton M (2005) Eye in the sky: tracking harmful algal blooms with satellite remote sensing. Water Atmos 13:14–15

    Google Scholar 

  • Clinton EH, Elif D, Kathryn JC, Cary SC, David LK, David AH (2005) A bacterium that inhibits the growth of Pfiesteria piscicida and other dinophytoplankton. Harmful Algae 4:221–234

    Article  Google Scholar 

  • Cundliffe E, McQuillen K (1976) Bacterial protein synthesis: the effects of antibiotics. J Mol Biol 30:137–146

    Article  Google Scholar 

  • Fernandez-Munoz R, Monro E, Torres-Pinedo R, Vazquez D (1971) Substrate- and antibiotic-binding sites at the peptidyl-transferase centre of Escherichia coli ribosomes. Studies on the chloramphenicol, lincomycin and erythromycin sites. Eur J Biochem 23:185–193

    Article  CAS  Google Scholar 

  • Fukami K, Nishijima T, Ishida Y (1997) Stimulative and inhibitory effects of bacteria on the growth of microalgae. Hydrobiologia 358:185–191

    Article  Google Scholar 

  • Fukami K, Yuzawa A, Nishijima T, Hata Y (1992) Isolation and properties of a bacterium inhibiting the growth of Gymnodinium nagasakiense. Nihon Suisan Gakkai-shi 58:1073–1077

    Google Scholar 

  • Furuki M, Kobayashi M (1991) Interaction between Chattonella and bacteria and prevention of this red tide. Mar Pollut Bull 23:189–193

    Article  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR–LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    CAS  Google Scholar 

  • Hallengraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

    Google Scholar 

  • Holmstrom C, Kjelleberg S (1999) Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30:285–293

    CAS  Google Scholar 

  • Iizuka S (1972) Gymnodinium type-’65 red tide occurring in anoxic environment of Omura Bay. Bull Plank Soc Jpn 19:22–33

    Google Scholar 

  • Ikeda T, Inoue Y, Suehiro A, Ikeshoji H, Ishida T, Takiguchi N, Kuroda A, Kato J, Ohtake H (2002) The effects of cyclodextrins on autoinducer activities of quorum sensing in Pseudomonas aeruginosa. J Incl Phenom Macrocycl Chem 44:381–382

    Article  CAS  Google Scholar 

  • Imai I, Ishida Y, Hata Y (1993) Killing of marine phytoplankton by gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan. Mar Biol 116:527–532

    Article  Google Scholar 

  • Imai I, Sunahara T, Nishikawa T, Hori Y, Kondo R, Hiroishi, S (2001) Fluctuations of the red tide algae Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in the Seto Inland Sea. Mar Biol 138:1043–1049

    Article  CAS  Google Scholar 

  • Itoh K, Imai I (1987) Raphidophyceae. In: Japan Fisheries Resource Conservation Association (ed) A guide for studies of red tide organisms. Shuwa, Tokyo, pp 122–130

    Google Scholar 

  • Iwata Y, Sugahara I, Kimura T, Kowa H, Matsumoto A, Noritake K (2004) Properties of an algicidal bacterium (Flavobacterium sp.) against Karenia mikimotoi isolated from Ise Bay, Japan. Nippon Suisan Gakkaishi 70:537–541

    Article  Google Scholar 

  • Kato J, Ikeda T, Kuroda A, Takiguchi N, Ohtake H (1999) Influence of Pseudoalteromonas sp. A28 extracellular products on the synthesis of proteases exhibiting lytic activity toward marine algae. In: Abstracts of the 99th General Meeting of American Society for Microbiology, Washington, District of Columbia, USA, Abstract 104

  • Kogure K, Simidu U, Taga N (1979) A tentative direct microscopic method for counting living marine bacteria. Can J Microbiol 25:415–420

    Article  CAS  Google Scholar 

  • Lee HK, Chun J, Moon EY, Ko SH, Lee DS, Lee HS, Bae KS. (2001) Hahella chejuensis gen. nov., sp. nov., an extracellular-polysaccharide-producing marine bacterium. Int J Syst Evol Microbiol 51:661–666

    CAS  Google Scholar 

  • Lee SO, Kato J, Takiguchi N, Kuroda A, Ikeda T, Mitsutani A, Ohtake H (2000) Involvement of an extracellular protease in algicidal activity of the marine bacterium Pseudoalteromonas sp. strain A28. Appl Environ Microbiol 66:4334–4339

    Article  CAS  Google Scholar 

  • Lewis SM, Corpe WA (1964) Prodigiosin-producing bacteria from marine sources. Appl Microbiol 12:13–17

    CAS  Google Scholar 

  • Lovejoy C, Bowman JP, Hallegraeff GM (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

    CAS  Google Scholar 

  • Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144

    Article  Google Scholar 

  • Na G, Choi W, Chun Y (1996) A study on red tide control with Loess suspension. J Aquacult 9:239–245

    Google Scholar 

  • Nakashima T, Kurachi M, Kato Y, Yamaguchi K, Oda T (2005a) Characterization of bacterium isolated from the sediment at coastal area of Omura bay in Japan and several biological activities of pigment produced by this isolate. Microbiol Immunol 49:407–415

    CAS  Google Scholar 

  • Nakashima T, Tamura T, Kurachi M, Yamaguchi K, Oda T (2005b) Apoptosis-mediated cytotoxicity of prodigiosin-like red pigment produced by γ-proteobacterium and its multiple bioactivities. Biol Pharm Bull 28:2289–2295

    Article  CAS  Google Scholar 

  • Oda T, Ishimatsu A, Shimada M, Takeshita S, Muramatsu T (1992) Oxygen-radical-mediated toxic effects of the red tide phytoplankton Chattonella marina on Vibrio alginolyticus. Mar Biol 112:505–509

    Article  CAS  Google Scholar 

  • Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, Hoiby N, Givskov M, Molin S, Eberl L (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249–3262

    CAS  Google Scholar 

  • Salmond GPC, Bycroft BW, Stewart GSAB, Williams P (1995) The bacterial enigma: cracking the code of cell–cell communication. Mol Microbiol 16:615–624

    Article  CAS  Google Scholar 

  • Sawabe T, Makino H, Tatsumi M, Nakano K, Tajima K, Iqbal MM, Yumoto I, Ezura Y, Christen R (1998) Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int J Syst Bacteriol 48:769–774

    Article  CAS  Google Scholar 

  • Sellner KG, Doucette GJ, Kirkpatrick GJ (2003) Harmful algal blooms: causes, impacts and detection. J Ind Microbiol Biotechnol 30:383–406

    Article  CAS  Google Scholar 

  • Shieh WY, Chen YW, Chaw SM, Chiu HH (2003) Vibrio ruber sp. nov., a red, facultatively anaerobic, marine bacterium isolated from sea water. Int J Syst Evol Microbiol 53:479–484

    Article  Google Scholar 

  • Skerratt JH, Bowman JP, Hallegraeff G, James S, Nichols PD (2002) Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Mar Ecol Prog Ser 244:1–15

    Google Scholar 

  • Steidinger KA (1993) A re-evaluation of toxic dinoflagellate biology and ecology. Prog Phycol Res 2:147–188

    Google Scholar 

  • Swift S, Throup JP, Salmond GPC, Williams P, Stewart GSAB (1996) Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem Sci 21:214–219

    Article  CAS  Google Scholar 

  • Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GPC (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36:539–556

    Article  CAS  Google Scholar 

  • Wang X, Gong L, Liang S, Han X, Zhu C, Li Y (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4:433–443

    Article  CAS  Google Scholar 

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Correspondence to Takuji Nakashima.

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Nakashima, T., Miyazaki, Y., Matsuyama, Y. et al. Producing mechanism of an algicidal compound against red tide phytoplankton in a marine bacterium γ-proteobacterium . Appl Microbiol Biotechnol 73, 684–690 (2006). https://doi.org/10.1007/s00253-006-0507-2

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  • DOI: https://doi.org/10.1007/s00253-006-0507-2

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