A Novel Algicide: Evidence of the Effect of a Fatty Acid Compound from the Marine Bacterium, Vibrio sp. BS02 on the Harmful Dinoflagellate, Alexandrium tamarense
Alexandrium tamarense is a notorious bloom-forming dinoflagellate, which adversely impacts water quality and human health. In this study we present a new algicide against A. tamarense, which was isolated from the marine bacterium Vibrio sp. BS02. MALDI-TOF-MS, NMR and algicidal activity analysis reveal that this compound corresponds to palmitoleic acid, which shows algicidal activity against A. tamarense with an EC50 of 40 μg/mL. The effects of palmitoleic acid on the growth of other algal species were also studied. The results indicate that palmitoleic acid has potential for selective control of the Harmful algal blooms (HABs). Over extended periods of contact, transmission electron microscopy shows severe ultrastructural damage to the algae at 40 μg/mL concentrations of palmitoleic acid. All of these results indicate potential for controlling HABs by using the special algicidal bacterium and its active agent.
References
[1]
Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean & coastal management 52: 342–347. doi: 10.1016/j.ocecoaman.2009.04.006
[2]
Ni L, Acharya K, Hao X, Li S (2012) Isolation and identification of an anti-algal compound from Artemisia annua and mechanisms of inhibitory effect on algae. Chemosphere 88: 1051–1057. doi: 10.1016/j.chemosphere.2012.05.009
[3]
Anderson DM, Kulis DM, Qi YZ, Zheng L, Lu S, et al. (1996) Paralytic shellfish poisoning in southern China. Toxicon 34: 579–590. doi: 10.1016/0041-0101(95)00158-1
[4]
Sala MM, Balagué V, Pedrós-Alió C, Massana R, Felipe J, et al. (2006) Phylogenetic and functional diversity of bacterioplankton during Alexandrium spp. blooms. FEMS Microbiology Ecology 54: 257–267. doi: 10.1016/j.femsec.2005.04.005
[5]
Zhang H, An X, Zhou Y, Zhang B, Li D, et al. (2013) Effect of oxidative stress induced by Brevibacterium sp. BS01 on a HAB causing species-Alexandrium tamarense. PLOS ONE8(5): e63018. doi: 10.1371/journal.pone.0063018
[6]
Xu D, Gao Z, Zhang X, Fan X, Wang Y, et al. (2012) Allelopathic interactions between the opportunistic species Ulva prolifera and the native macroalga Gracilaria lichvoides. PLoS One 7: e33648. doi: 10.1371/journal.pone.0033648
[7]
Bernbom N, Ng YY, Kjelleberg S, Harder T, Gram L (2011) Marine bacteria from Danish coastal waters show antifouling activity against the marine fouling bacterium Pseudoalteromonas sp. strain S91 and zoospores of the green alga Ulva australis independent of bacteriocidal activity. Appl Environ Microbiol 77: 8557–8567. doi: 10.1128/aem.06038-11
[8]
Kodani S, Imoto A, Mitsutani A, Murakami M (2002) Isolation and identification of the antialgal compound, harmane (1-methyl-β-carboline), produced by the algicidal bacterium, Pseudomonas sp. K44–1. Journal of applied phycology 14: 109–114.
[9]
Yang C, Li Y, Zhou Y, Zheng W, Tian Y, et al. (2012) Bacterial community dynamics during a bloom caused by Akashiwo sanguinea in the Xiamen Sea Area, China. Harmful algae 20: 132–141. doi: 10.1016/j.hal.2012.09.002
[10]
Kim YM, Wu Y, Duong TU, Jung SG, Kim SW, et al. (2012) Algicidal Activity of Thiazolidinedione Derivatives Against Harmful Algal Blooming Species. Marine Biotechnology: 1–11.
[11]
Sun XX, Han KN, Choi JK, Kim EK (2004) Screening of surfactants for harmful algal blooms mitigation. Marine pollution bulletin 48: 937–945. doi: 10.1016/j.marpolbul.2003.11.021
[12]
Jeong HJ, Kim HR, Kim KI, Kim KY, Park KH, et al. (2002) NaOCl produced by electrolysis of natural seawater as a potential method to control marine red-tide dinoflagellates. Phycologia 41: 643–656. doi: 10.2216/i0031-8884-41-6-643.1
[13]
Pan G, Chen J, Anderson DM (2011) Modified local sands for the mitigation of harmful algal blooms. Harmful algae 10: 381–387. doi: 10.1016/j.hal.2011.01.003
[14]
Tang Y, Zhang H, Liu X, Cai D, Feng H, et al. (2011) Flocculation of harmful algal blooms by modified attapulgite and its safety evaluation. Water research 45: 2855–2862. doi: 10.1016/j.watres.2011.03.003
[15]
Anderson D, Andersen P, Bricelj V, Cullen J, Rensel J (2001) Monitoring and Management Strategies for Harmful Algal Blooms in Coastal Waters, APEC· 201-MR-01.1. Asia Pacific Economic Program, Singapore, and Interguvernamental Oceanographyc Commission Technical Series, Paris: 268.
[16]
Secher S (2009) Measures to Control Harmful Algal Blooms. The Plymouth Student Scientist 2: 212–227.
[17]
Su J, Yang X, Zhou Y, Zheng TL (2011) Marine bacteria antagonistic to the harmful algal bloom species Alexandrium tamarense (Dinophyceae). Biological Control 56: 132–138. doi: 10.1016/j.biocontrol.2010.10.004
[18]
Jeong HJ, Kim JS, Yoo YD, Kim ST, Song JY, et al. (2008) Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful algae 7: 368–377. doi: 10.1016/j.hal.2007.12.004
[19]
Anderson DM (1997) Turning back the harmful red tide. Nature 338: 513–514.
[20]
Bai SJ, Huang LP, Su JQ, Tian Y, Zheng TL (2011) Algicidal Effects of a Novel Marine Actinomycete on the Toxic Dinoflagellate Alexandrium tamarense. Current Microbiology 62: 1774–1781. doi: 10.1007/s00284-011-9927-z
[21]
Cai W, Wang H, Tian Y, Chen F, Zheng TL (2011) Influence of a Bacteriophage on the Population Dynamics of Toxic Dinoflagellates by Lysis of Algicidal Bacteria. Applied and Environmental Microbiology 77: 7837–7840. doi: 10.1128/aem.05783-11
[22]
Zheng X, Zhang B, Zhang J, Su J, Yun Y, et al. (2013) A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Applied Microbiology and Biotechnology. 2013,97, (20), 9207–9215. doi: 10.1007/s00253-012-4617-8
[23]
Paul C, Pohnert G (2011) Interactions of the Algicidal Bacterium Kordia algicida with Diatoms: Regulated Protease Excretion for Specific Algal Lysis. PLoS One 6: e21032. doi: 10.1371/journal.pone.0021032
[24]
Wang BX, Yang XR, Zhou YY, Lv JL, Su JQ, et al. (2012) An algicidal protein produced by bacterium isolated from the Donghai Sea, China. Harmful Algae 20: 83–88. doi: 10.1016/j.hal.2011.10.006
[25]
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51: 139–144. doi: 10.1111/j.1550-7408.2004.tb00538.x
[26]
toxin production of a red-tide causing alga. Marine pollution bulletin 51: 1018–1025. doi: 10.1016/j.marpolbul.2005.02.039
[27]
Kim JD, Kim JY, Park JK, Lee CG (2009) Selective Control of the Prorocentrum minimum Harmful Algal Blooms by a Novel Algal-Lytic Bacterium Pseudoalteromonas haloplanktis AFMB-008041. Marine Biotechnology 11: 463–472. doi: 10.1007/s10126-008-9167-9
[28]
Chen WM, Sheu FS, Sheu SY (2012) Aquimarina salinaria sp. nov., a novel algicidal bacterium isolated from a saltpan. Arch Microbiol 194: 103–112. doi: 10.1007/s00203-011-0730-9
[29]
Choi H, Kim B, Kim J, Han M (2005) Streptomyces neyagawaensis as a control for the hazardous biomass of Microcystis aeruginosa (Cyanobacteria) in eutrophic freshwaters. Biological Control 33: 335–343. doi: 10.1016/j.biocontrol.2005.03.007
[30]
Su JQ, Yang XR, Zheng TL, Tian Y, Jiao NZ, et al. (2007) Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful algae 6: 799–810. doi: 10.1016/j.hal.2007.04.004
[31]
Wang BX, Zhou YY, Bai SJ, Su JQ, Tian Y, et al. (2010) A novel marine bacterium algicidal to the toxic dinoflagellate Alexandrium tamarense. Lett Appl Microbiol 51: 552–557. doi: 10.1111/j.1472-765x.2010.02936.x
[32]
Keawtawee T, Fukami K, Songsangjinda P (2012) Use of a Noctiluca-killing bacterium Marinobacter salsuginis strain BS2 to reduce shrimp mortality caused by Noctiluca scintillans. Fisheries Science 78: 641–646. doi: 10.1007/s12562-012-0497-1
[33]
Fu L, An X, Li D, Zhou L, Tian Y, et al. (2011) Isolation and alga-inhibiting characterization of Vibrio sp. BS02 against Alexandrium tamarense. World Journal of Microbiology and Biotechnology 27: 2949–2956. doi: 10.1007/s11274-011-0778-3
[34]
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. New York: Plenum Press. 29–60 p.
[35]
Bake SH, Sun XX, Lee YJ, Wang SY, Han KN, et al. (2003) Mitigation of harmful algal blooms by sophorolipid. Journal of microbiology and biotechnology 13: 651–659.
[36]
Lee SO, Kato J, Takiguchi N, Kuroda A, Ikeda T, et al. (2000) Involvement of an extracellular protease in algicidal activity of the marine bacterium Pseudoalteromonas sp. strain A28. Appl Environ Microbiol 66: 4334–4339. doi: 10.1128/aem.66.10.4334-4339.2000
[37]
Chen WM, Sheu FS, Sheu SY (2011) Novel L-amino acid oxidase with algicidal activity against toxic cyanobacterium Microcystis aeruginosa synthesized by a bacterium Aquimarina sp. Enzyme Microb Technol 49: 372–379. doi: 10.1016/j.enzmictec.2011.06.016
[38]
DeCosta P, Anil AC (2012) The effect of antibiotics on diatom communities. Current Science 102: 1552–1559.
[39]
Kawano Y, Nagawa Y, Nakanishi H, Nakajima H, Matsuo M, et al. (1997) Production of thiotropocin by a marine bacterium, Caulobacter sp. and its antimicroalgal activities. Journal of Marine Biotechnology 5: 225–229.
[40]
Kim D, Lee JS, Park YK, Kim JF, Jeong H, et al. (2007) Biosynthesis of antibiotic prodiginines in the marine bacterium Hahella chejuensis KCTC 2396. J Appl Microbiol 102: 937–944. doi: 10.1111/j.1365-2672.2006.03172.x
[41]
Alamsjah MA, Hirao S, Ishibashi F, Fujita Y (2005) Isolation and structure determination of algicidal compounds from Ulva fasciata. Biosci Biotechnol Biochem 69: 2186–2192. doi: 10.1271/bbb.69.2186
[42]
Nakai S, Yamada S, Hosomi M (2005) Anti-cyanobacterial fatty acids released from Myriophyllum spicatum. Hydrobiologia 543: 71–78. doi: 10.1007/s10750-004-6822-7
[43]
Oh MY, Lee SB, Jin DH, Hong YK, Jin HJ (2010) Isolation of algicidal compounds from the red alga Corallina pilulifera against red tide microalgae. Journal of applied phycology 22: 453–458. doi: 10.1007/s10811-009-9478-x
[44]
Ikawa M, Sasner JJ, Haney JF (1994) Lipids of cyanobacterium Aphanizomenon flos-aquae and inhibition of Chlorella growth. Journal of chemical ecology 20: 2429–2436. doi: 10.1007/bf02033211
[45]
Takamura Y, Yamada T, Kimoto A, Kanehama N, Tanaka T, et al. (2004) Growth inhibition of Microcystis cyanobacteria by L-lysine and disappearance of natural Microcystis blooms with spraying. Microbes and Environments 19: 31–39. doi: 10.1264/jsme2.19.31
[46]
Pokrzywinski KL, Place AR, Warner ME, Coyne KJ (2012) Investigation of the algicidal exudate produced by Shewanella sp. IRI-160 and its effect on dinoflagellates. Harmful algae 19: 23–29. doi: 10.1016/j.hal.2012.05.002
[47]
Kang YH, Kim JD, Kim BH, Kong DS, Han MS (2005) Isolation and characterization of a bio-agent antagonistic to diatom, Stephanodiscus hantzschii. J Appl Microbiol 98: 1030–1038. doi: 10.1111/j.1365-2672.2005.02533.x
[48]
Gumbo JR, Cloete TE (2011) The mechanism of Microcystis aeruginosa death upon exposure to Bacillus mycoides. Physics and Chemistry of the Earth, Parts A/B/C 36: 881–886. doi: 10.1016/j.pce.2011.07.050
[49]
Darehshouri A, Affenzeller M, Lutz-Meindl U (2008) Cell death upon H(2)O(2) induction in the unicellular green alga Micrasterias. Plant Biol (Stuttg) 10: 732–745. doi: 10.1111/j.1438-8677.2008.00078.x
[50]
Ozaki K, Ito E, Tanabe S, Natsume K, Tsuji K, et al. (2009) Electron microscopic study on lysis of a cyanobacterium Microcystis. Journal of Health Science 55: 578–585. doi: 10.1248/jhs.55.578
[51]
Alamsjah MA, Ishibe K, Kim D, Yamaguchi K, Ishibashi F, et al. (2007) Selective toxic effects of polyunsaturated fatty acids derived from Ulva fasciata on red tide phyotoplankter species. Bioscience, biotechnology, and biochemistry 71: 265–268. doi: 10.1271/bbb.60475
[52]
Wu JT, Chiang YR, Huang WY, Jane WN (2006) Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aquatic Toxicology 80: 338–345. doi: 10.1016/j.aquatox.2006.09.011
[53]
Yang X, Deng S, De Philippis R, Chen L, Hu C, et al. (2012) Chemical composition of volatile oil from Artemisia ordosica and its allelopathic effects on desert soil microalgae, Palmellococcus miniatus. Plant Physiol Biochem 51: 153–158. doi: 10.1016/j.plaphy.2011.10.019
[54]
Kamaya Y, Kurogi Y, Suzuki K (2003) Acute toxicity of fatty acids to the freshwater green alga Selenastrum capricornutum. Environmental toxicology 18: 289–294. doi: 10.1002/tox.10127
[55]
Alamsjah MA, Hirao S, Ishibashi F, Oda T, Fujita Y (2009) Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. Developments in Applied Phycology 2: 263–270. doi: 10.1007/978-1-4020-9619-8_33
[56]
Chiang IZ, Huang WY, Wu JT (2004) Allelochemicals of botryococcus braunii (chlorophyceae) 1. Journal of phycology 40: 474–480. doi: 10.1111/j.1529-8817.2004.03096.x
[57]
Hirao S, Tara K, Kuwano K, Tanaka J, Ishibashi F (2012) Algicidal activity of glycerolipids from brown alga Ishige sinicola toward red tide microalgae. Biosci Biotechnol Biochem 76: 372–374. doi: 10.1271/bbb.110645
[58]
Takamura Y, Chino M, Osada A, Nishihara H, Yagi O (1999) Growth responses of Microcystis and Oscillatoria cyanobacteria to various organic compounds and growth inhibition by L-lysine and L-histidine. Environmental Science 12: 329–337.
