Ocean Science Journal

, Volume 46, Issue 2, pp 105–115 | Cite as

Interactions between the pathogenic bacterium Vibrio parahaemolyticus and red-tide dinoflagellates

Open Access


Vibrio parahaemolyticus is a common pathogenic bacterium in marine and estuarine waters. To investigate interactions between V. parahaemolyticus and co-occurring redtide dinoflagellates, we monitored the daily abundance of 5 common red tide dinoflagellates in laboratory culture; Amphidinium carterae, Cochlodinium ploykrikoides, Gymnodinium impudicum, Prorocentrum micans, and P. minimum. Additionally, we measured the ingestion rate of each dinoflagellate on V. parahaemolyticus as a function of prey concentration. Each of the dinoflagellates responded differently to the abundance of V. parahaemolyticus. The abundances of A. carterae and P. micans were not lowered by V. parahaemolyticus, whereas that of C. polykrikodes was lowered considerably. The harmful effect depended on bacterial concentration and incubation time. Most C. polykrikoides cells died after 1 hour incubation when the V. parahaemolyticus concentration was 1.4×107 cells ml−1, while cells died within 2 days of incubation when the bacterial concentration was 1.5×106 cells ml−1. With increasing V. parahaemolyticus concentration, ingestion rates of P. micans, P. minimum, and A. carterae on the prey increased, whereas that on C. polykrikoides decreased. The maximum or highest ingestion rates of P. micans, P. minimum, and A. carterae on V. parahaemolyticus were 55, 5, and 2 cells alga−1 h−1, respectively. The results of the present study suggest that V. parahaemolyticus can be both the killer and prey for some red tide dinoflagellates.

Key words

algicidal bacteria feeding harmful algal bloom ingestion red tide 


  1. Amaro AM, Fuentes MS, Ogalde SR, Venegas JA, Suarez BA (2005) Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagella Alexandrium catenella. J Eukary Microb 52(3): 191–200CrossRefGoogle Scholar
  2. Andersen RJ, Wolfe MS, Faulkner DJ (1974) Autotoxic antibiotic production by a marine Chromobacterium. Mar Biol 27:281–285CrossRefGoogle Scholar
  3. Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696CrossRefGoogle Scholar
  4. Bienfang PK, DeFelice SV, Laws EA, Brand LE, Bidigare RR, Christensen S, Trapido-Rosenthal H, Hemscheidt TK, McGillicuddy Jr DJ, Anderson DM, Solo-Gabriele HM, Boehm AB, Backer LC (2011) Prominent human health impacts from several marine microbes: history, ecology, and public health implications. Int J Microb 2011:152815. doi:10.1155/2011/152815Google Scholar
  5. Byun HG, Jeong SY, Park YT, Lee WJ, Kim SK (2002) Algicidal activity of substance purified from marine bacteria metabolites against Cochlodinium polykrikoides. J Fish Sci Tech 5(3):150–155Google Scholar
  6. Dadisman TA Jr, Nelson R, Molenda JR, Garber HJ (1972) Vibrio parahaemolyticus gastroenteritis in Maryland I. Clinical and epidemiologic aspects. Am J Epidemiol 96(6):414–426Google Scholar
  7. Doucette GJ, Kodama M, Franca S, Gallacher S (1998) Bacterial interactions with harmful algal bloom species: bloom ecology, toxigenesis, and cytology. In: Anderson DA, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms, Vol 41. Springer-Verlag, Heidelberg, pp 29–48Google Scholar
  8. Doucette GJ, McGovern ER, Babinchak JA (1999) Algicidal bacteria active against Gymnodinium breve(Dinophyceae). I. Bacterial isolation and characterization of killing activity. J Phycol 35:1447–1457CrossRefGoogle Scholar
  9. Eiler A, Johansson M, Bertilsson S (2006) Environmental influences on Vibrio populations in Northern temperate and boreal coastal waters (Baltic and Skagerrak Seas) Appl Environ Microb 72(9):6004–6011CrossRefGoogle Scholar
  10. Fraga S, Bravo I, Delgado M, Franco JM, Zapata M (1995) Gyrodinium impudicum sp.nov.(Dinophyceae), a non toxic, chain-forming, red tide dinoflagellate. Phycologia 34(6):514–521CrossRefGoogle Scholar
  11. Furusawa G, Yoshikawa T, Yasuda A, Sakata T (2003) Algicidal activity and gliding motility of Saprospira sp. SS98-5. Can J Microbiol 49:92–100CrossRefGoogle Scholar
  12. Fukami K, Yuzawa A, Nishijima T, Hata Y (1992) Isolation and properties of a bacterium inhibiting the growth of Gymnodinium nagasakiense. Nippon Suisan Gakkaishi 58(6):1073–1077Google Scholar
  13. Gárate-Lizárraga I, López-Cortes DJ, Bustillos-Guzmán JJ, Hemández-Sandoval F (2004) Blooms Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Rev Biol Trop 52(Suppl.1):51–58Google Scholar
  14. Green DH, Llewllyn LE, Negri AP, Blackburn SI, Bolch CJ (2004) Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish dinoflagellate Gymnodinium catenatum. FEMS Microbiol Ecol 47(3):345–357CrossRefGoogle Scholar
  15. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana (Hustedt) and Detonula confervacea (Cleve). Can J Microbiol 8:229–239CrossRefGoogle Scholar
  16. Hackett JD, Anderson DM, Erdner DM, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534CrossRefGoogle Scholar
  17. Hare CE, Demir E, Coyne KJ, Cary SC, Kirchman DL, Hutchins DA (2005) A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful algae 4:221–234CrossRefGoogle Scholar
  18. Hervio-Heath D, Colwell RR, Derrien A, Robert-Pillot A, Fournier JM, Pommepuy M (2002) Occurrence of pathogenic vibrios in coastal areas of France. J Appl microbiol 92(6):1123–1135CrossRefGoogle Scholar
  19. Holmstrom C, Kjelleberg S (1999) Marine Psedoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30:285–293Google Scholar
  20. Imai I, Ishida Y, Hata Y (1993) Killing of marine phytoplankton by a gliding bacterium Cytophaga sp. isolated from the coastal sea of Japan. Mar Biol 116:527–532CrossRefGoogle Scholar
  21. Imai I, Ishida Y, Sakaguchi K, Hata Y (1995) Algicidal marine bacteria isolated from northern Hiroshima Bay, Japan. Fish Sci Tokyo 61(4):628–636Google Scholar
  22. Imai I, Sunahara T, Nishikawa T, Hori Y, Kondo R, Hiroishi S (2001) Fluctuation of the red tide flagellates Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in the Seto Inland Sea. Mar Biol 138:1043–1049CrossRefGoogle Scholar
  23. Imai I, Kimura S (2008) Resistance of the fish-killing dinoflagellate Cochlodinium polykrikoides against algicidal bacteria islolated from the coastal sea of Japan. Harmful algae 7:360–367CrossRefGoogle Scholar
  24. Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN (2005) Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl Environ Microbiol 71(7):3483–3494CrossRefGoogle Scholar
  25. Jeong SY, Park YT, Lee WJ (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 Korean Fish Soc 33(4):331–338Google Scholar
  26. Jeong HJ, Kim HR, Kim KI, Kim KY, Park KH, Kim ST, Yoo YD, Song JY, Seong KA, Yih WH, Pae SJ, Lee CH, Huh MD, Lee SH (2002) NaOCl produced by electrolysis of natural seawater as a potential method to control marine red tide dinoflagellates. Phycologia 45:643–656CrossRefGoogle Scholar
  27. Jeong HJ, Kim JS, Yoo YD, Kim ST, Song JY, Kim TH, Seong KA, Kang NS, Kim MS, Kim JH, Kim S, Ryu J, Lee HM, Yih WH (2008) Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7:368–377CrossRefGoogle Scholar
  28. Kim MC, Yu HS, Ok MS, Kim CH, and Chang DS (1999) The activities and characteristics of algicidal bacteria in Chindong Bay. J Korean Fish Soc 32(3):359–367Google Scholar
  29. Kim DI, Matsuyama Y, Mineo SN, Yoon YH, Oshima Y (2004) Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef(Dinophyceae). J Plankton Res 26:61–66CrossRefGoogle Scholar
  30. Kim CJ, Kim HG, Kim CH, Oh HM (2007) Life cycle of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters. Harmful algae 6(1):104–111CrossRefGoogle Scholar
  31. Kim D, Kim JF, Yim JH, Kwon SK, Lee CH (2008) Red to redthe marine bacterium Hahella chejuensis and its product prodigiosin for mitigation of harmful algal blooms. J Microbiol Biotechnol 18(10):1621–1629Google Scholar
  32. Kim JD, Kim JH, Park JK, Lee CG (2009) Selective control of the Prorocentrum minimum harmful algal blooms by a novel algal-Lytic bacterium Psedoalteromonas haloplanktis AFMB-008041. Mar Biotechnol 11:463–472CrossRefGoogle Scholar
  33. Kitaguchi H, Hiragushi N, Mitsutani A, Yamaguchi M, Ishida Y (2001) Isolation of an algicidal marine bacterium with activity against the harmful dinoflagellate Heterocapsa circularisquama (Dinophyceae). Phycologia 40(3):275–279CrossRefGoogle Scholar
  34. Lee WJ, Kim HG, Park YT, Seong HI(1990) The role of marine bacteria in the dinoflagellate bloom. Bull Korean Fish Soc 23(4):303–309Google Scholar
  35. Lee WJ, Park YT (1998) Isolation of marine bacteria killing red tide microalgae. II: isolation and algicidal properties of Psedomonas sp. LG-2 possessing killing activity for dinoflagellate, Prorocentrum micans. J Korean Fish Soc 31(6):852–858Google Scholar
  36. Lee BK, Katano T, Kitamura SI, Oh MJ, Han MS (2008) Monitoring of algicidal bacterium, Alteromonas sp. Strain A14 in its application to natural Cochlodinium polykrikoides blooming seawater using fluorescence in situ hybridization. J Microbiol 46(3):274–282CrossRefGoogle Scholar
  37. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, lijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, lida T (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholera. The Lancet 361(9359):743–749CrossRefGoogle Scholar
  38. Manage PM, Kawabata Z, Nakano SI (2000) Algicidal effect of the bacterium Alcaligenes denirificans on Microcystis spp. Aquat Microb Ecol 22(2):111–117CrossRefGoogle Scholar
  39. Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 5(2):139–144CrossRefGoogle Scholar
  40. Nakashima T, Kim D, Miyazaki Y, Yamaguchi K, Takeshita S, Oda T (2006) Mode of action of an antialgal agent produced by a marine gamma Proteobacterium against Chattonella marina. Aquat Microb Ecol 45:255–262CrossRefGoogle Scholar
  41. National Fisheries Research and Development Institute (NFRDI) (1998) Red tides in Korea. National Fisheries Research & Development Institute, Korea, 292 pGoogle Scholar
  42. Nayak BB, Karunasagar I, Karunasagar I (2000) The survival of different Vibrios in association with a laboratory culture of the red-tide-causing organism Amphidinium carterae. World J Microbiol Biotechnol 16:99–101CrossRefGoogle Scholar
  43. Nygaard K, Tobiesen A (1993) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38:273–279CrossRefGoogle Scholar
  44. Park YT, Park JB, Chung SY, Song BC, Lim WA, Kim CH, Lee WJ (1998) Isolation of marine bacteria killing red tide microalgae. I. Isolation and algicidal properties of Micrococcus sp. LG-1 possessing killing activity for harmful dinoflagellate, Cochlodinium polykrikoides. J Korean Fish Soc 31(5):767–773Google Scholar
  45. Richlen MM, Morton SL, Jamali EA, Rajan A, Anderson DM (2010) The catastrophic 2008–2009 red tide in the Arabian gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful algae 9:163–172CrossRefGoogle Scholar
  46. Roberts KR, Heimann K, Wetherbee R (1995) The flagellar apparatus and canal structure in Prorocentrum micans (Dinophyceae). Phycologia 34(4):313–322CrossRefGoogle Scholar
  47. Romalde JL, Torazo AE, Barja JL (1990) Changes in bacterial populations during red tides caused by Mesodinium rubrum and Gymnodinium catenatum in North-West coast of Spain. J Appl Bacteriol 68:123–132Google Scholar
  48. Seong KA, Jeong HJ, Kim S, Kim GH, Kang JH (2006) Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marine bacteria. Mar Eco Prog Ser 322:85–97CrossRefGoogle Scholar
  49. Sherr EB, Sherr EB, Fallon RD (1987) Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microb 53(5):958–965Google Scholar
  50. Skerratt JH, Bowman JP, Hallegraeff G, James S, Nichols PD (2002) Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Austalian estuary. Mar Ecol Prog Ser 244:1–15CrossRefGoogle Scholar
  51. Wang X, Gong L, Liang S, Han X, Zhu C, Li Y (2005) Algicidal activity of rhamnolipid biosurfactants produced by Psedomonas aeruginosa. Harmful algae 4:433–443CrossRefGoogle Scholar
  52. Wright AC, Shneider RG, Hubbard MA, Schneider KR (2009) Preventing foodborne and non-foodborne illness: Vibrio parahaemolyticus. University of Florida IFAS Extention FSHN09-01Google Scholar
  53. Yeung PS, Boor KJ (2004) Epidemiology, pathogenesis, and prevention of foodborn Vibrio parahaemolyticus infections. Foodborne Pathog Dis 1(2):74–88CrossRefGoogle Scholar

Copyright information

© Korea Ocean Research & Development Institute (KORDI) and the Korean Society of Oceanography (KSO) and Springer Netherlands 2011

Authors and Affiliations

  1. 1.Saemankeum Environmental Research CenterKunsan National UniversityKunsanKorea
  2. 2.School of Earth and Environmental Sciences, College of Natural SciencesSeoul National UniversitySeoulKorea

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