Abstract
Seagrasses are known to have allelopathic activity to reduce growth of phytoplankton. We found growth-inhibiting bacteria (strains E8 and E9) from Zostera marina possessing strong activity against the toxic dinoflagellate Alexandrium tamarense. Strain E9 markedly inhibited growth of A. tamarense even with initial inoculum size as small as 2.9 cells ml−1. This bacterium also had growth-inhibiting effects on the red-tide raphidophytes Chattonella antiqua and Heterosigma akashiwo, the dinoflagellate Heterocapsa circularisquama, and the diatom Chaetoceros mitra. Small subunit (SSU) ribosomal DNA (rDNA) sequencing analysis demonstrated that the most probable affiliation of these strains was Flavobacteriaceae, and proved that another inhibitory bacterial strain (E8) was the same species as strain E9. Two other bacterial strains (E4-2 and E10), showing different colony color and isolated from the same seagrass sample, revealed no growth-inhibiting activity. Interestingly, strain E4-2 showed the same sequences as E8 and E9 (100 %), and strain E10 matched E8 and E9 with 99.80 % similarity. Growth-inhibiting bacteria against the toxic dinoflagellate Alexandrium tamarense associated with seagrass, such as Flavobacterium spp. E8 and E9, are able to repress shellfish poisoning besides the allelopathic activity of seagrass itself.
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References
Anderson DM, Tilman JA, Allan DC, Yves C, Estelle M, Marina M (2012) The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35
Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99
Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Imai I, Ishida Y, Sawayama S, Hata Y (1991) Isolation of marine gliding bacterium that kills Chattonella antiqua (Raphidophycase). Nippon Suisan Gakkaishi 57:1409
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 116:527–532
Fukami K, Yuzawa T, Nishijima T, Hata Y (1992) Isolation and properties of a bacterium inhibiting the growth of Gymnodinium nagasakiense. Nippon Suisan Gakkaishi 58:1073–1077
Imai I, Kim MC, Nagasaki K, Itakura S, Ishida Y (1998) Relationships between dynamics of red tide-causing raphidophycean flagellates and algicidal micro-organism in the coastal sea of Japan. Phycol Res 46:139–146
Kim MC, Yoshinaga I, Imai I, Nagasaki K, Itakura S, Ishida Y (1998) A close relationship between algicidal bacteria and termination of Heterosigma akashiwo (Raphidophyceae) blooms in Hiroshima Bay, Japan. Mar Ecol Prog Ser 170:25–32
Fukami K, Nishijima T, Murata H, Doi S, Hata Y (1991) Distribution of bacteria influential on the development and the decay of Gymnodinium nagasakiense red tide and their effects on algal growth. Nippon Suisan Gakkaishi 57:2321–2326
Imai I, Sunahara T, Nishikawa T, Hori Y, Kondo R, Hiroishi S (2001) Fluctuations of the red tide flagellates Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in Seto Inland Sea, Japan. Mar Biol 138:1043–1049
Ferrier M, Martin JL, Rooney-Varga JN (2002) Stimulation of Alexandrium fundyense growth by bacterial assemblages from the Bay of Fundy. J Appl Microbiol 92:1–12
Yoshinaga I, Kawai T, Ishida Y (1997) Analysis of algicidal ranges of the bacteria killing the marine dinoflagellate Gymnodinium mikimotoi isolated from Tanabe Bay, Wakayama Pref, Japan. Fish Sci 63:94–98
Adachi M, Kanno T, Okamoto R, Itakura S, Yamaguchi M, Nishijima T (2003) Population structure of Alexandrium (Dinophyceae) cyst formation-promoting bacteria in Hiroshima Bay, Japan. Appl Environ Microbiol 69:6560–6568
Gallacher S, Flynn KJ, Franco JM, Buueggemann EE, Hines HB (1997) Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp. (Dynophyta) in culture. Appl Environ Microbiol 63:239–245
Nagai S, Imai I (1998) Enumeration of bacteria in seawater and sediment from the Seto Inland Sea of Japan that promote sperm formation in Coscinodiscus wailesii (Bacillariophyceae). Phycologia 37:363–368
Williams SL, Heck KL (2001) Seagrass community ecology. In: Bertness M et al (eds) Marine community ecology. Sinauer, Sunderland, pp 317–337
Duarte CM, Middelburg J, Caraco N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8
McGlathery KJ, Sundbäck K, Anderson IC (2007) Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Mar Ecol Prog Ser 348:1–18
Laabir M, Grignon-Dubois M, Cecchi P, Rezzonico B, Rouquette M, Masseret E (2010) Allelopathic effects of Zostera spp. on the growth and photosynthetic activity of the toxic dinoflagellate Alexandrium catenella. In: Proceedings of the 4th Mediterranean Symposium on Marine Vegetation. Regional Activity Center for Specially Protected Areas, Yasmine-Hammamet, pp 187–188
Wit R, Troussellier M, Courties C, Buffan-Dubau E, Lemaire E (2012) Short-term interactions between phytoplankton and intertidal seagrass vegetation in a coastal lagoon (Bassin d’Arcachon, SW France). Hydrobiologia 699:55–68
Imai I, Yamamoto T, Ishii K, Yamamoto K (2009) Promising prevention strategies for harmful red tides by seagrass beds as enormous sources of algicidal bacteria. In: Proceedings of 5th world fisheries congress. TERRAPUB, Tokyo, 6c_0995_133
Chen LCM, Edelstein T, McLachlan J (1969) Bonnemaisonia hamifera Hariot in nature and in culture. J Phycol 5:211–220
Imai I, Itakura S, Matsuyama Y (1996) Selenium requirement for growth of a novel red tide flagellate Chattonella verruculosa (Raphidophyceae) in culture. Fish Sci 62:834–835
Koch AL (1994) Growth measurement. In: Gerhardt P, Murray RGE, Wood WS, Krieg NR (eds) Methods for general molecular bacteriology. Am. Soc. Microbiol., Washington, DC, pp 248–277
Imai I, Kim MC, Nagasaki K, Itakura S, Ishida Y (1998) Detection and enumeration of microorganisms that are lethal to harmful phytoplankton in coastal waters. Plankton Biol Ecol 45:19–29
Ishida Y, Eguchi M, Kadota H (1986) Existence of obligatory oligotrophic bacteria as a dominant population in South China Sea and the west Pacific Ocean. Mar Ecol Prog Ser 30:197–203
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Kim YS, Lee DS, Jeong SY, Lee WJ, Lee MS (2009) Isolation and characterization of a marine algicidal bacterium against the harmful Raphidophyceae Chattonella marina. J Microbiol 47:9–18
Fukami K, Nishijima T, Ishida Y (1997) Stimulative and inhibitory effects of bacteria on the growth of microalgae. Hydrobiologia 358:185–191
Mayali X (2007) Bacterial influence on the bloom dynamics of the dinoflagellate Lingulodinium polyedrum. Scripps Institution of Oceanography Technical Report, Scripps Institution of Oceanography, University of California, San Diego, p 154
Mayali X, Franks PJS, Tanaka Y, Azam F (2008) Bacteria-induced motility reduction in Lingulodinium polyedrum (Dinophyceae). J Phycol 44:923–928
Su JQ, Yang XR, Zheng TL, Tian Y, Jiao NZ, Cai LZ, Hong HS (2007) Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 6:799–810
Su JQ, Xiaoru Y, Yanyan Z, Tianling Z (2011) Marine bacteria antagonistic to the harmful algal bloom species Alexandrium tamarense (Dinophyceae). Biol Control 56:132–138
Wang BX, Zhou YY, Bai SJ, Su JQ, Tian Y, Zheng TL, Yang XR (2010) A novel marine bacterium algicidal to the toxic dinoflagellate Alexandrium tamarense. Lett Appl Microbiol 51:552–557
Bai SJ, Huang LP, Su JQ, Tian Y, Zheng TL (2011) Algicidal effects of a novel marine actinomycete on the toxic dinoflagellate Alexandrium tamarense. Curr Microbiol 62:1774–1781
Amaro AM, Fuentes MS, Ogalde SR, Venegas JA, Suàerz-Isla AB (2005) Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J Eukaryot Microbiol 52:191–200
Nagasaki K, Yamaguchi M, Imai I (2000) Algicidal activity of a killerbacterium against the harmful red tide dinoflagellate Heterocapsa circularisquama isolated from Ago Bay, Japan. Nippon Suisan Gakkaishi 66:666–673 (in Japanese with English abstract)
Roth PB, Twiner MJ, Mikulski CM, Barnhorst AB, Doucette GJ (2008) Comparative analysis of two algicidal bacteria active against the red tide dinoflagellate Karenia brevis. Harmful Algae 7:682–691
Fistarol GO, Catherine L, Karin R, Edna G (2004) Temporary cyst formation in phytoplankton: a response to allelopathic competitors? Environ Microbiol 6:791–798
Lee SO, Kato J, Takiguchi T, 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
Wang B, Yang X, Lu J, Zhou Y, Su J, Tian Y, Zhang J, Wang G, Zheng T (2012) A marine bacterium producing protein with algicidal activity against Alexandrium tamarense. Harmful Algae 13:83–88
Imai I, Ishida Y, Sakaguchi K, Hata Y (1995) Algicidal marine bacteria isolated from northern Hiroshima Bay, Japan. Fish Sci 61:628–636
Liu J, Lewitus AJ, Kempton JW, Wilde SB (2008) The association of algicidal bacteria and raphidophyte blooms in South Carolina brackish detention ponds. Harmful Algae 7:184–193
Park JH, Yoshinaga I, Nishikawa T, Imai I (2008) Algicidal bacteria in particle-associated form and in free-living form during a diatom bloom in the Seto Inland Sea, Japan. Aquat Microb Ecol 60:151–161
Yoshinaga I, Kim MC, Katanozaka N, Imai I, Uchida A, Ishida Y (1998) Population structure of algicidal marine bacteria targeting the red tide forming alga Heterosigma akashiwo (Raphidophyceae), determined by restriction fragment length polymorphism analysis of the bacterial 16S ribosomal RNA genes. Mar Ecol Prog Ser 170:33–44
Imai I, Yamaguchi M (2012) Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella. Harmful Algae 14:46–70
Yanagi T (2008) “Sato-Umi”-A new concept for sustainable fisheries. In: Tsukamoto T et al (eds) Fisheries for global welfare and environment. TERRAPUB, Tokyo, pp 351–358
Costanza R, Arge R, Groot R, Farberk S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Suttonkk P, Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260
Watson RA, Coles RG, Leelong WJ (1993) Simulation estimates of annual yield and landed value for commercial penaeid prawns from a tropical seagrass habitat. Aust J Mar Freshw Res 44:211–219
Harrison PG, Chan AT (1980) Inhibition of the growth of micro-algae and bacteria by extracts of eelgrass (Zostera marina) leaves. Mar Biol 61:21–26
Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS 106:12377–12381
Abdenadher M, Hamza A, Fekih W, Hannachi I, Bellaaj AZ, Bradai MN, Aleya L (2012) Factors determining the dynamics of toxic blooms of Alexandrium minutum during a 10-year study along the shallow southwestern Mediterranean coasts. Estuar Coast Shelf Sci 106:102–111
Acknowledgments
We are grateful to Dr. Hiroyuki Munehara of Usujiri Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, for his kind arrangement of seagrass sampling. We thank Mr. Kiyoshi Nomura for his technical assistance for sampling at Usujiri Port. This study was supported in part by the project of Hakodate Green Innovation of UMI (Universal Marine Industry).
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Onishi, Y., Mohri, Y., Tuji, A. et al. The seagrass Zostera marina harbors growth-inhibiting bacteria against the toxic dinoflagellate Alexandrium tamarense . Fish Sci 80, 353–362 (2014). https://doi.org/10.1007/s12562-013-0688-4
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DOI: https://doi.org/10.1007/s12562-013-0688-4