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Isolation of AHL-degrading bacteria from micro-algal cultures and their impact on algal growth and on virulence of Vibrio campbellii to prawn larvae

  • Environmental biotechnology
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Abstract

Inactivation of quorum sensing (QS) signal molecules, such as acylhomoserine lactones (AHLs) of pathogenic bacteria, has been proposed as a novel method to combat bacterial diseases in aquaculture. Despite the importance of micro-algae for aquaculture, AHL degradation by bacteria associated with micro-algal cultures has thus far not been investigated. In this study, we isolated Pseudomonas sp. NFMI-T and Bacillus sp. NFMI-C from open cultures of the micro-algae Tetraselmis suecica and Chaetoceros muelleri, respectively. An AHL degradation assay showed that either monocultures or co-cultures of the isolates were able to degrade the AHL N-hexanoyl-l-homoserine lactone. In contrast, only Bacillus sp. NFMI-C was able to inactivate N-hydroxybutanoyl-l-homoserine lactone, the AHL produced by Vibrio campbellii. The isolated bacteria were able to persist for up to 3 weeks in conventionalized micro-algal cultures, indicating that they were able to establish and maintain themselves within open algal cultures. Using gnotobiotic algal cultures, we found that the isolates did not affect growth of the micro-algae from which they were isolated, whereas a mixture of both isolates increased the growth of Tetraselmis and decreased the growth of Chaetoceros. Finally, addition of Bacillus sp. NFMI-C to the rearing water of giant river prawn (Macrobrachium rosenbergii) larvae significantly improved survival of the larvae when challenged with pathogenic V. campbellii, whereas it had no effect on larval growth.

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References

  • Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bassler BL, Greenberg EP, Stevens AM (1997) Cross-species induction of luminescence in the quorum sensing bacterium Vibrio harveyi. J Bacteriol 179:4043–4045

    PubMed Central  CAS  PubMed  Google Scholar 

  • Boon N, De Windt W, Verstraete W, Top EM (2002) Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16 S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol Ecol 39:101–112

    CAS  PubMed  Google Scholar 

  • Bostock J, McAndrew B, Richards R, Jauncey K, Telfer T, Lorenzen K, Little D, Ross L, Handisyde N, Gatward I, Corner R (2010) Aquaculture: global status and trends. Phil Trans R Soc B365:2897–2912

    Article  Google Scholar 

  • Bruhn JB, Dalsgaard I, Nielsen KF, Buccholtz C, Larsen JL, Gram L (2005) Quorum sensing signal molecules (acylated homoserine lactones) in Gram-negative fish pathogenic bacteria. Dis Aquat Org 65:43–52

    Article  CAS  PubMed  Google Scholar 

  • Cam DTV, Hao NV, Dierckens K, Defoirdt T, Boon N, Sorgeloos P, Bossier P (2009a) Novel approach of using homoserine lactone-degrading and poly-beta-hydroxybutyrate-accumulating bacteria to protect Artemia from the pathogenic effects of Vibrio harveyi. Aquaculture 291:23–30

    Article  Google Scholar 

  • Cam DTV, Nhan DT, Ceuppens S, Hao NV, Dierckens K, Wille M, Sorgeloos P, Bossier P (2009b) Effect of N-acyl homoserine lactone-degrading enrichment cultures on Macrobrachium rosenbergii larviculture. Aquaculture 294:5–13

    Article  CAS  Google Scholar 

  • Cao YA, He SX, Zhou ZG, Zhang MC, Mao W, Zhang HT, Yao B (2012) Orally administered thermostable N-acyl homoserine lactonase from Bacillus sp strain AI96 attenuates Aeromonas hydrophila infection in zebrafish. Appl Environ Microbiol 78:1899–1908

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen RD, Zhou ZG, Cao BYG, Yao B (2010) High yield expression of an AHL-lactonase from Bacillus sp B546 in Pichia pastoris and its application to reduce Aeromonas hydrophila mortality in aquaculture. Microb Cell Factories 9:39

    Article  Google Scholar 

  • Chu W, Zhou S, Zhu W, Zhuang X (2014) Quorum quenching bacteria Bacillus sp. QSI-1 protect zebrafish (Danio rerio) from Aeromonas hydrophila infection. Sci rep 4:5446.DOI: 10.1038/srep05446

  • Defoirdt T, Boon N, Bossier P, Verstraete W (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240:69–88

    Article  Google Scholar 

  • Defoirdt T, Sorgeloos P, Bossier P (2011a) Alternatives to antibiotics for the control of bacterial diseases in aquaculture. Curr Opin Microbiol 14:251–258

    Article  PubMed  Google Scholar 

  • Defoirdt T, Thanh LD, Van Delsen B, De Schryver P, Sorgeloos P, Boon N, Bossier P (2011b) N-acylhomoserine lactone degrading Bacillus strains isolated from aquaculture animals. Aquaculture 311:258–260

    Article  CAS  Google Scholar 

  • Dong YH, Wang LH, Zhang LH (2007) Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc B362:1201–1211

    Article  Google Scholar 

  • FAO, 2013. Cultured aquatic species information programme. Macrobrachium rosenbergii.

  • Fast W, Tipton PA (2012) The enzymes of bacterial census and censorship. Trends Biochem Sci 37:7–14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freeman JA, Bassler BL (1999) Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J Bacteriol 181:899–906

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hargreaves JA (2006) Photosynthetic suspended-growth systems in aquaculture. Aquac Eng 34:344–363

    Article  Google Scholar 

  • http://www.fao.org/fishery/culturedspecies/Macrobrachium_rosenbergii/en. Accessed 27 March 2013

  • Kennedy B, Venugopal MN, Karunasagar I, Karunasagar I (2006) Bacterial flora associated with the giant freshwater prawn Macrobrachium rosenbergii, in the hatchery system. Aquaculture 261:1156–1167

    Article  Google Scholar 

  • LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77(1):73–111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maddox MB, Manzi JJ (1976) The effects of algal supplements on static system culture on Macrobrachium rosenbergii (de Man) larvae. Proc World Maricult Soc 7:677–698

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Molina L, Constantinescu F, Michel L, Reimmann C, Duffy B, Defago G (2003) Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol Ecol 45:71–81

    Article  CAS  PubMed  Google Scholar 

  • Morohoshi T, Inaba T, Kato N, Kanai K, Ikeda T (2004) Identification of quorum-sensing signal molecules and the LuxRI homologs in fish pathogen Edwardsiella tarda. J Biosci Bioeng 98:274–281

    Article  CAS  PubMed  Google Scholar 

  • Natrah FMI, Bossier P, Sorgeloos P, Yusoff FM, Defoirdt T (2014) Significance of microalgal-bacterial interactions for aquaculture. Rev Aquacult 5:1–14

    Google Scholar 

  • New MB, Valenti WC, Tidwell JH, D’Abramo LR, Kutty MN (2010) Freshwater prawn: biology and farming. Blackwell Publishing Ltd

  • Nhan DT, Cam DTV, Wille M, Defoirdt T, Bossier P, Sorgeloos P (2010) Quorum quenching bacteria protect Macrobrachium rosenbergii larvae from Vibrio harveyi infection. J Appl Microbiol 109:1007–1016

    Article  CAS  PubMed  Google Scholar 

  • Pande GSJ, Natrah FMI, Sorgeloos P, Bossier P, Defoirdt T (2013) The Vibrio harveyi quorum sensing signals have a different impact on virulence of the bacterium towards different hosts. Vet Microbiol 167:540–545

    Article  CAS  PubMed  Google Scholar 

  • Ruwandeepika HAD, Jayaweera TSP, Bhowmick PP, Karunasagar I, Bossier P, Defoirdt T (2012) Pathogenesis, virulence factors and virulence regulation of vibrios belonging to the Harveyi clade. Rev Aquacult 4:59–74

    Article  Google Scholar 

  • Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK., Chhabra SR, Williams P, Macintyre S, Stewart GSAB (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 179:5271–5281

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tang K, Zhang XH (2014) Quorum quenching agents: resources for antivirulence therapy. Mar Drugs 12:3245–3282. doi:10.3390/md12063245

    Article  PubMed Central  PubMed  Google Scholar 

  • Tinh NTN, Gunasekara RAYSA, Boon N, Dierckens K, Sorgeloos P, Bossier P (2007) N-acyl homoserine lactone-degrading microbial enrichment cultures isolated from Penaeus vannamei shrimp gut and their probiotic properties in Brachionus plicatilis cultures. FEMS Microbiol Ecol 62:45–53

    Article  CAS  PubMed  Google Scholar 

  • Tinh NTN, Yen VHN, Dieckens K, Sorgeloos P, Bossier P (2008) An acyl homoserine lactone-degrading microbial community improves the survival of first-feeding turbot larvae (Scophthalmus maximus L.). Aquaculture 285:56–62

    Article  CAS  Google Scholar 

  • Tonguthai K (1997) Diseases of the freshwater prawn, Macrobrachium rosenbergii. Aquat Anim Health Res Inst Newslett 4:1–9

    Google Scholar 

  • Wang YB, Li JR, Lin J (2008) Probiotics in aquaculture: challenges and outlook. Aquaculture 281:1–4

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the Research Foundation of Flanders (FWO-Vlaanderen; project no. 1.5.013.12N), by the Bijzonder Onderzoeksfonds (BOF)—special research fund for a PhD finalization grant from Ghent University (Code: 01DI0114) and by the Directorate General of Higher Education of Indonesia through a doctoral scholarship to G.S.J.P. by the University Putra Malaysia and Malaysian Ministry of Higher Education (MOHE) through doctoral grant to N.F.M.I.

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Laboratory of Aquaculture & Artemia Reference Center, Ghent University, Rozier 44, B-9000, Ghent, Belgium

    Gde Sasmita Julyantoro Pande, Ace Vincent Bravo Flandez, Uday Kumar, Yufeng Niu, Peter Bossier & Tom Defoirdt

  2. Department of Aquatic Resources Management, Faculty of Marine Science and Fisheries, Udayana University, Bali, Indonesia

    Gde Sasmita Julyantoro Pande

  3. Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, Serdang, Malaysia

    Fatin Mohd Ikhsan Natrah

  4. Laboratory of Marine Biotechnology, Universiti Putra Malaysia, Serdang, Selangor, Malaysia

    Fatin Mohd Ikhsan Natrah

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  1. Gde Sasmita Julyantoro Pande
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  2. Fatin Mohd Ikhsan Natrah
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  3. Ace Vincent Bravo Flandez
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  4. Uday Kumar
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  5. Yufeng Niu
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  6. Peter Bossier
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  7. Tom Defoirdt
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Correspondence to Tom Defoirdt.

Additional information

Gde Sasmita Julyantoro Pande and Fatin Mohd Ikhsan Natrah contributed equally to this work.

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Pande, G.S.J., Natrah, F.M.I., Flandez, A.V.B. et al. Isolation of AHL-degrading bacteria from micro-algal cultures and their impact on algal growth and on virulence of Vibrio campbellii to prawn larvae. Appl Microbiol Biotechnol 99, 10805–10813 (2015). https://doi.org/10.1007/s00253-015-6918-1

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