Skip to main content

Advertisement

Log in

A potential bacterial biocontrol agent, strain S2V2 against pathogenic marine Vibrio in aquaculture

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

We isolated a marine bacterium strain S2V2 which inhibited the growth of pathogenic marine Vibrio spp. The aims of this research were to identify a new antibiotic-producing marine bacterium strain S2V2, and evaluate its spectrum activity and pathogenic property. Analysis of 16S rDNA sequence placed strain S2V2 in the genus Pseudoalteromonas, but the sequence similarity was low (95.46%) implying the strain might be a new species in this genus. Strain S2V2 inhibited the growth of 67.9% of 28 Vibrio strains tested. This strain inhibited V. alginolyticus, V. anguillarum, V. fluvialis, V. harveyi, V. metschnikovii, V. splendidus, V. ordalii, V. parahaemolyticus, and V. vulnificus, but inactive against V. campbellii, Aeromonas hydrophyla and Staphylococcus aureus. Strain S2V2 produced extracellular non proteinaceous antibacterial substances. The highest antibacterial activity was found when strain S2V2 was cultured for 96 h in ZoBell broth medium. An artificial infection to post larvae of Lithopenaeus vanname indicated that strain S2V2 was a non pathogenic bacterium. Non pathogenic property and specific antibacterial activity against a broad range of fish pathogenic marine Vibrio of strain S2V2 suggest that this strain is a prospective source of unique antibiotic and a potential biocontrol agent in marine aquaculture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alcaide E, Blasco M-D, Esteve C (2005) Occurrence of drug-resistant bacteria in two European eel farms. Appl Environ Microbiol 71:3348–3350. doi:10.1128/AEM.71.6.3348-3350.2005

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    CAS  Google Scholar 

  • Aoki T (2000) Transferable drug resistance plasmids in fish-pathogenic bacteria. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of chemicals in aquaculture in Asia. SEAFDEC, Iloilo, pp 31–34 ISBN 971-8511-49-0

    Google Scholar 

  • Aoki T, Satoh T, Kitao T (1987) New tetracycline resistance determinant on R plasmids from Vibrio anguillarum. Antimicrob Agents Chemother 31:1446–1449

    CAS  Google Scholar 

  • Austin B, Austin DA (1993) Bacterial fish pathogens: diseases in farmed and wild fish, 2nd edn. Ellis Horwood Ltd., Chichester, pp 265–294

    Google Scholar 

  • Benbrook CM (2002) Antibiotic drug use in US aquaculture: information available on the world wide web. http://www.healthobservatory.org/library.cfm?RefID=37397. Accessed 14 Jan 2009

  • Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805

    Article  CAS  Google Scholar 

  • Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144. doi:10.1111/j.1462-2920.2006.01054.x

    Article  CAS  Google Scholar 

  • Dang H, Zhang X, Song L, Chang Y, Yang G (2007) Molecular determination of oxytetracycline-resistant bacteria and their resistance genes from mariculture environments of China. J App Microbiol 103:2580–2592. doi:10.1111/j.1365-2672.2007.03494.x

    Article  CAS  Google Scholar 

  • Del Castillo CS, MdI Wahid, Yoshikawa T, Sakata T (2008) Isolation and inhibitory effect of anti-Vibrio substances from Pseudoalteromonas sp. A1–J11 isolated from the coastal sea water of Kagoshima Bay. Fish Sci 74:174–179

    Article  CAS  Google Scholar 

  • Esposito A, Fabrizi L, Lucchetti D, Marvasi L, Coni E, Guandalini E (2007) Orally administered erythromycin in rainbow trout (Oncorhynchus mykiss): residues in edible tissues and withdrawal time. Antimicrob Agents Chemother 51:1043–1047. doi:10.1128/AAC.01002-06

    Article  CAS  Google Scholar 

  • Esteve C, Amaro C, Biosca EG, Garay E (1995) Biochemical and toxigenic properties of Vibrio furnissii isolated from a European eel farm. Aquaculture 132:81–90. doi:10.1016/0044-8486(94)00381-W

    Article  Google Scholar 

  • Franks A, Haywood P, Holmström C, Egan S, Kjelleberg S, Kumar N (2005) Isolation and structure elucidation of a novel yellow pigment from the marine bacterium Pseudoalteromonas tunicata. Molecules 10:1286–1291

    Article  CAS  Google Scholar 

  • Gauthier MJ (1976) Alteromonas rubra sp. nov., a new marine antibiotic-producing bacterium. Int J Syst Bacteriol 26:459–466

    Google Scholar 

  • Gauthier MJ (1982) Validation of the name Alteromonas luteoviolacea. Int J Syst Bacteriol 32:82–86

    Google Scholar 

  • Gauthier MJ, Breittmayer VA (1979) A new antibiotic-producing bacterium from seawater: Alteromonas aurantia sp.nov. Int J Syst Bacteriol 29:366–372

    Google Scholar 

  • GESAMP (IMO/FAO/Unesco/WMO/WHO/IAEA/UN/UNEP Joint Group of Experts on the Scientific Aspects of Marine Pollution) (1991) Reducing environmental impacts of coastal aquaculture. GESAMP Reports and Studies No. 47:32p. http://www.fao.org/DOCREP/006/u3100e/U3100e00.htm

  • Gómez-León J, Villamil L, Lemos ML, Novoa B, Figueras A (2005) Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured Carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Appl Environ Microbiol 71:98–104. doi:10.1128/AEM.71.1.98-104.2005

    Article  CAS  Google Scholar 

  • Hameed ASS, Rahaman KH, Alagan A, Yoganandhan K (2003) Antibiotic resistance in bacteria isolated from hatchery-reared larvae and post-larvae of Macrobrachium rosenbergii. Aquaculture 217:39–48. doi:10.1016/S0044-8486(02)00298-3

    Article  Google Scholar 

  • Hanefeld U, Floss HG, Laatsch H (1994) Biosynthesis of the marine antibiotic pentabromopseudilin: 1. The benzene ring. J Org Chem 59:3604–3608

    Article  CAS  Google Scholar 

  • Holmström K, Gräslund S, Wahlström A, Poungshompoo S, Bengtsson B-E, Kautsky N (2003) Antibiotic use in shrimp farming and implications for environmental impacts and human health. Int J Food Sci Technol 38:255–266. doi:10.1046/j.1365-2621.2003.00671.x

    Article  Google Scholar 

  • Horikawa M, Noro T, Kamei Y (1999) In vitro anti-methicillin resistant Staphylococcus aureus activity found in extract of marine algae indigenous to the coastline of Japan. J Antibiot 52:182–189

    Google Scholar 

  • Inglis V (2000) Antibacterial chemotherapy in aquaculture: review of practice, associated risks and need for action. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of chemicals in aquaculture in Asia. SEAFDEC, Iloilo, pp 7–22 ISBN 971-8511-49-0

    Google Scholar 

  • Isnansetyo A, Kamei Y (2003a) MC21-A, a bactericidal antibiotic produced by a new marine bacterium, Pseudoalteromonas phenolica sp. nov., against methicillin-resistant Staphylococcus aureus (MRSA). Antimicrob Agents Chemother 47:480–488. doi:10.1128/AAC.47.2.480-488.2003

    Article  CAS  Google Scholar 

  • Isnansetyo A, Kamei Y (2003b) Pseudoalteromonas phenolica sp. nov., a novel marine bacterium that produces phenolic anti-methicillin-resistant Staphylococcus aureus (MRSA) substances. Int J Syst Evol Microbiol 53:583–588. doi:10.1099/ijs.0.02431-0

    Article  CAS  Google Scholar 

  • Isnansetyo A, Kamei Y (2005) Direct antagonistic method for screening anti-methicillin-resistant Staphylococcus aureus (MRSA) substance-producing marine bacteria. Biota 10:141–145

    Google Scholar 

  • Ivanova EP, Sawabe T, Lysenko AM, Gorshkova NM, Svetashev VI, Nicolau DV, Yumoto N, Taguchi T, Yoshikawa S, Christen R, Mikhailov VV (2002a) Pseudoalteromonas ruthenica sp. nov., isolated from marine invertebrates. Int J Syst Bacteriol 52:235–240

    Google Scholar 

  • Ivanova EP, Shevchenko LS, Sawabe T, Lysenko AM, Svetashev VI, Gorshkova NM, Satomi M, Christen R, Mikhailov VV (2002b) Pseudoalteromonas maricaloris sp. nov., isolated from an Australian sponge, reclassification of [Pseudoalteromonas aurantia] NCIMB 2033 as Pseudoalteromonas flavipulchra sp. nov. Int J Sys Evol Microbiol 52:263–271

    CAS  Google Scholar 

  • James S, Holmström C, Kjelleberg S (1996) Purification and characterisation of a novel antibacterial protein from the marine bacterium D2. Appl Environ Microbiol 62:2783–2788

    CAS  Google Scholar 

  • Kalinovskaya NI, Ivanova EP, Alexeeva YV, Gorshkova NM, Kuznetsova TA, Dmitrenok AS, Nicolau DV (2004) Low-molecular-weight, biologically active compounds from marine Pseudoalteromonas species. Curr Microbiol 48:441–446

    Article  CAS  Google Scholar 

  • Kalinovskaya NI, Dmitrenok AS, Kuznetsova TA, Frolova GM, Christen R, Laatsch H, Alexeeva YV, Ivanova EP (2008) ‘‘Pseudoalteromonas januaria’’ SUT 11 as the source of rare lipodepsipeptides. Curr Microbiol 56:199–207

    Article  CAS  Google Scholar 

  • Kalmokoff MP, Lanthier T-L, Tremblay M, Foss PC, Lau G, Sanders J, Austin J, Szymanski JM (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188:4312–4320. doi:10.1128/JB.01975-05

    Article  CAS  Google Scholar 

  • Kamiso HN, Isnansetyo A, Triyanto, Istiqomah I, Murdjani M (2005) Isolation, identification and characterization of pathogenic Vibrio spp. causative agents of vibriosis in grouper at brackishwater Aquaculture Development Centre, Situbondo. J Fish Sci VII:80–94

    Google Scholar 

  • Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet SA (2001) A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Org 46:139–145. doi:10.3354/dao046139

    Article  CAS  Google Scholar 

  • Lalumera GM, Calamari D, Galli P, Castiglioni S, Crosa G, Fanelli R (2004) Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere 54:661–668. doi:10.1016/j.chemosphere.2003.08.001

    Article  CAS  Google Scholar 

  • Lee TX, Munekage Y, Kato S (2005) Antibiotic resistance in bacteria from shrimp farming in mangrove areas. Sci Total Environ 349:95–105. doi:10.1016/j.scitotenv.2005.01.006

    Article  CAS  Google Scholar 

  • Lunder T, Sørum H, Holstad G, Steigerwalt AG, Mowinckel P, Brenner DJ (2000) Phenotypic and genotypic characterization of Vibrio viscosus sp. nov. and Vibrio wodanis sp. nov. isolated from Atlantic salmon (Salmo salar) with ‘winter ulcer’. Int J Sys Evol Microbiol 50:427–450

    CAS  Google Scholar 

  • McCann J, Stabb EV, Millikan DS, Ruby EG (2003) Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl Environ Microbiol 69:5928–5934. doi:10.1128/AEM.69.10.5928-5934.2003

    Article  CAS  Google Scholar 

  • McCarthy SA, Johnson RM, Kakimoto D, Sakata T (1985) Effects of various agents on the pigment (violacein) and antibiotic production of Alteromonas luteoviolacea. Bull Jap Soc Sci Fish 51:1115–1121

    Google Scholar 

  • Nakayama Y, Hayashi M, Yoshikawa K, Mochida K, Unemoto T (1999) Inhibitor studies of new antibiotic, korormicin, 2-n-hepthyl-4-hydroxyquinoline N-oxide and Ag+ toward the Na+ -translocating NADH quinine reductase from Vibrio alginolyticus. Biol Pharm Bull 22:1064–1067

    CAS  Google Scholar 

  • Nelson EJ, Ghiorse WC (1999) Isolation and identification of Pseudoalteromonas piscicida strain Cura-d associated with diseased damselfish (Pomacentridae) eggs. J Fish Dis 22:253–260. doi:10.1046/j.1365-2761.1999.00168.x

    Article  Google Scholar 

  • Nicolas JL, Corre S, Gauthier G, Robert R, Ansquer D (1996) Bacterial problems associated with scallop Pecten maximus larval culture. Dis Aquat Org 27:67–76. doi:10.3354/dao027067

    Article  Google Scholar 

  • Nonaka L, Isshiki T, Suzuki S (2000) The occurrence of oxytetracycline resistant bacteria in the fish intestine and seawater environment. Microbes Environ 15:223–228

    Article  Google Scholar 

  • Ottaviani D, Bacchiocchi I, Masini L, Leoni F, Carraturo A, Giammarioli M, Sbaraglia G (2001) Antimicrobial susceptibility of potentially pathogenic halophilic vibrios isolated from seafood. Int J Antimicrobial Agents 18:135–140. doi:10.1016/S0924-8579(01)00358-2

    Article  CAS  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  Google Scholar 

  • Pedersen K, Verdonck L, Austin B, Austint DA, Blancht AR, Grimont PAD, Jofre J, Koblavi S, Larsen JL, Tiainen T, Vigneulle M, Swings J (1998) Taxonomic evidence that Vibrio carchariae Grimes et al. 1985 is a junior synonym of Vibrio harveyi (Johnson and Shunk 1936) Baumann et al. 1981. Intl J Syst Bacteriol 48:749–758

    CAS  Google Scholar 

  • Planas M, Pérez-Lorenzo M, Hjelm M, Gram L, Fiksdal IU, Bergh Ø, Pintado J (2006) Probiotic effect in vivo of Roseobacter strain 27-4 against Vibrio (Listonella) anguillarum infections in turbot (Scophthalmus maximus L.) larvae. Aquaculture 255:323–333. doi:10.1016/j.aquaculture.2005.11.039

    Article  Google Scholar 

  • Pujalte MJ, Sitjà-Bobadilla A, Macián MC, Álvarez-Pellitero P, Garay E (2007) Occurrence and virulence of Pseudoalteromonas spp. in cultured gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Molecular and phenotypic characterisation of P. undina strain U58. Aquaculture 271:47–53. doi:10.1016/j.aquaculture.2007.06.015

    Article  Google Scholar 

  • Robertson PAW, Dowd CO, Burrells C, Williams P, Austin B (2000) Use of Carnobacterium sp. as a probiotic for Atlantic salmon_Salmo salar L. and rainbow trout, Oncorhynchus mykiss, Walbaum. Aquaculture 185:235–243. doi:10.1016/S0044-8486(99)00349-X

    Article  Google Scholar 

  • Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Sarter S, Nguyen HNK, Hung LT, Lazard J, Montet D (2007) Antibiotic resistance in Gram-negative bacteria isolated from farmed catfish. Food Control 18:1391–1396

    Article  CAS  Google Scholar 

  • Sinhaseni P, Limpoka M, Samatiwat O (2000) Human health aspects of the use of chemicals in aquaculture, with special emphasis on food safety and regulations. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of chemicals in aquaculture in Asia. SEAFDEC, Iloilo, pp 55–60 ISBN 971-8511-49-0

    Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general, molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  • Smith SK, Sutton DC, Fuerst JA, Reichelt JL (1991) Evaluation of the genus Listonella and reassignment of Listonella damsela (Love et al.) MacDonell and Colwell to the genus Photobacterium as Photobacterium damsela comb. nov. with an emended description. Intl J Syst Bacteriol 41:529–534

    CAS  Google Scholar 

  • Sobolevskaya MP, Smetanina OF, Speitling M, Shevchenko LS, Dmitrenok PS, Laatsch H, Kuznetsova TA, Ivanova EP, Elyakov GB (2005) Controlling production of brominated cyclic depsipeptides by Pseudoalteromonas maricaloris KMM 636T. Lett App Microbiol 40:243–248

    Article  CAS  Google Scholar 

  • Stackerbrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  Google Scholar 

  • Sugumar G, Nakai T, Hirata Y, Matsubara D, Muroga K (1998) Vibrio splendidus biovar I1 as the causative agent of bacillary necrosis of Japanese oyster Crassostrea gigas larvae. Dis Aquat Org 33:111–118. doi:10.3354/dao033111

    Article  CAS  Google Scholar 

  • Tall BD, Fall S, Pereira MR, Ramos-Valle M, Curtis SK, Kothary MH, Chu DMT, Monday SR, Kornegay L, Donkar T, Prince D, Thunberg RL, Shangraw KA, Hanes DE, Khambaty FM, Lampel KA, Bier JW, Bayer RC (2003) Characterization of Vibrio fluvialis-like strains implicated in limp lobster disease. Appl Environ Microbiol 69:7435–7446. doi:10.1128/AEM.69.12.7435-7446.2003

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Tjahjadi MR, Angka SL, Suwanto A (1994) Isolation and evaluation of marine bacteria for biocontrol of luminous bacterial disease in tiger shrimp larvae (Panaeus monodon, Fab.). Asia Pac J Mol Biol Biotechnol 2:347–352

    Google Scholar 

  • Urzúa A, Jara F, Tojo E, Wilkens M, Mendoza L, Rezende MC (2006) A new antibacterial clerodane diterpenoid from the resinous exudate of Haplopappus uncinatus. J Ethnopharmacol 103:297–301. doi:10.1016/j.jep.2005.09.042

    Article  CAS  Google Scholar 

  • Vaseeharan B, Ramasamya P, Muruganc T, Chenb JC (2005) In vitro susceptibility of antibiotics against Vibrio spp. and Aeromonas spp. isolated from Penaeus monodon hatcheries and ponds. Int J Antimicrobial Agents 26:285–291. doi:10.1016/j.ijantimicag.2005.07.005

    Article  CAS  Google Scholar 

  • Venkateswaran K, Dohmoto N (2000) Pseudoalteromonas peptidolytica sp. nov., a novel mussel-thread-degrading bacterium isolated from the Sea of Japan. Int J Syst Evol Microbiol 50:565–574

    CAS  Google Scholar 

  • Vijayan KK, Singh ISB, Jayaprakash NS, Alavandi SV, Pai SS, Preetha R, Rajan JJS, Santiago TC (2006) A brackishwater isolate of Pseudomonas PS-102, a potential antagonistic bacterium against pathogenic vibrios in penaeid and non-penaeid rearing systems. Aquaculture 251:192–200. doi:10.1016/j.aquaculture.2005.10.010

    Article  CAS  Google Scholar 

  • Villamil L, Figueras A, Planas M, Novoa B (2003) Control of Vibrio alginolyticus in Artemia culture by treatment with bacterial probiotics. Aquaculture 219:43–56. doi:10.1016/S0044-8486(02)00515-X

    Article  Google Scholar 

  • Weston DP (2000) Ecological effects of the use of chemicals in aquaculture. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of chemicals in aquaculture in Asia. SEAFDEC, Iloilo, pp 23–30 ISBN 971-8511-49-0

    Google Scholar 

  • Yoshikawa K, Takadera T, Adachi K, Nishijima M, Sano H (1997) Korormicin, a novel antibiotic specifically active against marine gram negative bacteria, produced by a marine bacterium. J Antibiot 50:949–953

    CAS  Google Scholar 

  • Zanetti S, Spanu T, Deriu A, Romano L, Sechi LA, Fadda G (2001) In vitro susceptibility of Vibrio spp. isolated from the environment. Int J Antimicrobial Agents 17:407–409. doi:10.1016/S0924-8579(01)00307-7

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Identification of strain S2V2 was financially supported by a grant from Directorate of Higher Education, Department of National Education, the Republic of Indonesia under Fundamental Research Program (Contract number: LPPM-UGM/568/2007). We thank to the Laboratory of Fish and Environment Health, Brackishwater Aquaculture Development Center, Jepara, Indonesia for the gift of V. harveyi isolate.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alim Isnansetyo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Isnansetyo, A., Istiqomah, I., Muhtadi et al. A potential bacterial biocontrol agent, strain S2V2 against pathogenic marine Vibrio in aquaculture. World J Microbiol Biotechnol 25, 1103–1113 (2009). https://doi.org/10.1007/s11274-009-9992-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-009-9992-7

Keywords

Navigation