Skip to main content

Advertisement

SpringerLink
Log in

Disruption of Bacterial Cell-to-Cell Communication by Marine Organisms and its Relevance to Aquaculture

  • Review
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Bacterial disease is one of the most critical problems in commercial aquaculture. Although various methods and treatments have been developed to curb the problem, yet they still have significant drawbacks. A novel and environmental-friendly approach in solving this problem is through the disruption of bacterial communication or quorum sensing (QS). In this communication scheme, bacteria regulate their own gene expression by producing, releasing, and sensing chemical signals from the environment. There seems to be a link between QS and diseases through the regulation of certain phenotypes and the induction of virulence factors responsible for pathogen–host association. Several findings have reported that numerous aquatic organisms such as micro-algae, macro-algae, invertebrates, or even other bacteria have the potential to disrupt QS. The mechanism of action varies from degradation of signals through enzymatic or chemical inactivation to antagonistic as well as agonistic activities. This review focuses on the existing marine organisms that are able to interfere with QS with potential application for aquaculture as bacterial control.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

QS:

Quorum sensing

QSI:

Quorum sensing inhibitor(y)

References

  • Bachère E (2003) Anti-infectious immune effectors in marine invertebrates: potential tools for disease control in larviculture. Aquaculture 227:427–438

    Google Scholar 

  • Bao W-Y, Satuito CG, Yang J-L, Kitamura H (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Mar Biol 150:565–574

    Google Scholar 

  • Baruah K, Cam DTV, Dierckens K, Wille M, Defoirdt T, Sorgeloos P, Bossier P (2009) In vivo effects of single or combined N-acyl homoserine lactone quorum sensing signals on the performance of Macrobrachium rosenbergii larvae. Aquaculture 288:233–238

    CAS  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  CAS  Google Scholar 

  • Bi ZX, Liu YJ, Lu CP (2007) Contribution of AhyR to virulence of Aeromonas hydrophila. J Res Vet Sci 83:150–156

    CAS  Google Scholar 

  • Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, McCoy WF (2001) Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl Environ Microb 67(7):3174–3179

    CAS  Google Scholar 

  • Boyer M, Wisniewski-Dyé F (2009) Cell–cell signaling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1–19

    PubMed  CAS  Google Scholar 

  • Brackman G, Celen S, Baruah K, Bossier P, Van Calenbergh S, Nelis HJ, Coenye T (2009) AI-2 quorum sensing inhibitors affect the starvation response and reduce virulence in several Vibrio species, most likely by interfering with LuxPQ. Microbiology+ 155:4114–4122

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Buch C, Sigh J, Nielsen J, Larsen JL, Gram L (2003) Production of acylated homoserine lactones by different serotypes of Vibrio anguillarum both in culture and during infection of rainbow trout. Syst Appl Microbiol 26:338–349

    PubMed  CAS  Google Scholar 

  • Buchholtz C, Nielsen KF, Milton DL, Larsen JL, Gram L (2006) Profiling of acylated homoserine lactones of Vibrio anguillarum in vitro and in vivo: influence of growth conditions and serotype. Syst Appl Microbiol 29:433–445

    PubMed  CAS  Google Scholar 

  • Byers JT, Lucas C, Salmond GPC, Welch M (2002) Non enzymatic turnover of an Erwinia carotovora quorum sensing signaling molecule. J Bacteriol 184:1163–1171

    PubMed  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(7):1137–1144

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Cao JG, Meighen EA (1989) Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem 264:21670–21676

    PubMed  CAS  Google Scholar 

  • Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL (2002) Structural identification of a bacterial quorum sensing containing boron. Nature 415:545–549

    PubMed  CAS  Google Scholar 

  • Clark BR, Engene N, Teasdale ME, Rowley DC, Matainaho T, Valeriote FA, Gerwick WH (2008) Natural products chemistry and taxonomy of the marine cyanobacterium Blennothrix cantharidosmum. J Nat Prod 71:1530–1537

    PubMed  CAS  Google Scholar 

  • Croxatto A, Chalker AJ, Lauritz J, Jass J, Hardman A, Williams P, Cámara M, Milton DL (2002) VanT, a homoloque of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment and biofilm production in Vibrio anguillarum. J Bacteriol 184(6):1617–1629

    PubMed  CAS  Google Scholar 

  • Czajkowski R, Jafra S (2009) Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol 56:1–16

    PubMed  CAS  Google Scholar 

  • Darshanee Ruwandeepika HA, Defoirdt T, Bhowmick PP, Karunasagar I, Karunasagar I, Bossier P (2010) In vitro and in vivo expression of virulence genes in Vibrio isolates belonging to the Harveyi clade in relation to their virulence towards gnotobiotic brine shrimp (Artemia franciscana) Environ Microbiol. doi:10.1111/j.1462-2920.2010.02354

  • Das S, Ward LR, Burke C (2008) Prospects of using marine actinobacteria as probiotics in aquaculture. Appl Microbiol Biotechnol 81:419–429

    PubMed  CAS  Google Scholar 

  • Daume S, Brand-Gardner S, Woelkerling WJ (1999) Preferential settlement of abalone larvae: diatom films vs. non-geniculate coralline red algae. Aquaculture 174:243–254

    Google Scholar 

  • De Kievit TR, Iglewski BH (2000) Bacterial quorum sensing in pathogenic relationships. Infect Immun 68(9):4839–4849

    PubMed  Google Scholar 

  • Defoirdt T, Boon N, Bossier P, Verstraete W (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240:69–68

    Google Scholar 

  • Defoirdt T, Bossier P, Sorgeloos P, Verstraete W (2005) The impact of mutations in the quorum sensing systems of Aeromonas hydrophila, Vibrio anguillarum and Vibirio harveyi on their virulence towards gnotobiotically cultured Artemia franciscana. Environ Microbiol 7:1239–1247

    PubMed  CAS  Google Scholar 

  • Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W, Bossier P (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbelii and Vibrio paraheaemolyticus isolates. Appl Environ Microbiol 72(9):6419–6423

    PubMed  CAS  Google Scholar 

  • Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2007a) Alternatives to antibiotics to control bacterial infections—luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25:472–479

    PubMed  CAS  Google Scholar 

  • Defoirdt T, Miyamoto CM, Wood TK, Meighen EA, Sorgeloos P, Verstraete W, Bossier P (2007b) The natural furanone (5Z)-4 bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone disrupts quorum sensing-regulated gene expression in Vibrio harveyi by decreasing the DNA-binding activity of the transcriptional regulator protein luxR. Environ Microbiol 9(10):2486–2495

    PubMed  CAS  Google Scholar 

  • Defoirdt T, Ruwandeepika HAD, Karunasagar I, Boon N, Bossier P (2010) Quorum sensing negatively regulates chitinase in Vibrio harveyi. Environ Microbiol Rep 2:44–49

    Google Scholar 

  • Denkin SM, Nelson DR (2004) Regulation of Vibrio anguillarum empA metalloprotease expression and its role in virulence. Appl Environmen Microbiol 70(7):4193–4204

    CAS  Google Scholar 

  • Dobretsov SV, Dahms H-W, YiLi H, Wahl M, Qian P-Y (2007) The effect of quorum-sensing blockers on the formation of marine microbial communities and larval attachment. FEMS Microbiol Ecol 60:177–188

    PubMed  CAS  Google Scholar 

  • Donabedian H (2003) Quorum sensing and its relevance to infectious disease. J Infect 46:207–214

    PubMed  CAS  Google Scholar 

  • Dong Y-H, Zhang L-H (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43:101–109

    PubMed  CAS  Google Scholar 

  • Dong Y-H, Gusti AR, Zhang Q, Zu JL, Zhang L-H (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759

    PubMed  CAS  Google Scholar 

  • Dong Y-H, Wang LH, Zhang L-H (2007) Quorum-quenching microbial infections: mechanisms and implications. Philos T R Soc B 362:1201–1211

    CAS  Google Scholar 

  • Duarte CM, Marbá N, Holmer M (2007) Rapid domestication of marine species. Science 316:382–383

    PubMed  CAS  Google Scholar 

  • Dudler R, Elberl E (2006) Interactions between bacteria and eukaryotes via small molecules. Curr Opin Biotechnol 17:268–273

    PubMed  CAS  Google Scholar 

  • Dworjanyn SA, Steinberg P (1999) Localisation and surface quantitation of secondary metabolites in the red alga Delisea pulchra. Mar Biol 133:727–736

    CAS  Google Scholar 

  • FAO (2009) State of world fisheries and aquaculture 2009. FAO Fisheries Department. Food and Agriculture Organisation of the United Nations, Rome, Italy

    Google Scholar 

  • Funke M, Buchler R, Mahobia V, Schneeberg A, Ramm M, Boland W (2008) Rapid hydrolysis of quorum-sensing molecules in the gut of lepidopteran larvae. Chem Bio Chem 9:1953–1959

    PubMed  CAS  Google Scholar 

  • García-Aljaro C, Eberl L, Riedel K, Blanch AR (2008) Detection of quorum-sensing related molecules in Vibrio scopthalmi. BMC Microbiol 8:138

    PubMed  Google Scholar 

  • Givskov M, De Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD, Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling. J Bacteriol 178:6618–6622

    PubMed  CAS  Google Scholar 

  • Gram L, de Nys R, Maximilien R, Givskov SP, Kjelleberg S (1996) Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Appl Environm Microbiol 62(11):4284–4287

    CAS  Google Scholar 

  • Guglielmetti E, Korhonen JM, Heikkinen J, Morelli L, von Wrigh A (2009) Transfer of plasmid-mediated resistance to tetracycline in pathogenic bacteria from fish and aquaculture environments. FEMS Microbiol Lett 293:28–34

    PubMed  CAS  Google Scholar 

  • Han Y, Li X, Qi Z, Zhang X-H, Bossier P (2009) Detection of different quorum-sensing signal molecules in a virulent Edwardsiella tarda strain LTB-4. J Appl Microbiol 108:139–147

    Google Scholar 

  • Henke JM, Bassler BL (2004a) Three parallel quorum sensing systems regulate gene expression in V. harveyi. J Bacteriol 186:6902–6914

    CAS  Google Scholar 

  • Henke JM, Bassler BL (2004b) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186(12):3794–3805

    CAS  Google Scholar 

  • Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft J-U (2007) Does efficiency sensing unify diffusion and quorum sensing. Nat Rev Microbiol 5:230–239

    PubMed  CAS  Google Scholar 

  • Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristofferson P, Manefield M, Costerton JW, Moiln S, Eberl L, Steinberg P, Kjelleberg S, Hoiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815

    PubMed  CAS  Google Scholar 

  • Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL (2007) The major Vibrio cholera autoinducer and its role in virulence factor production. Nature 450:883–886

    PubMed  CAS  Google Scholar 

  • Huang Y-L, Dobretsov S, Ki J-S, Yang L-H, Qian P-Y (2007) Presence of acyl-homoserine lactone in subtidal biofilm and the implication in larval behavioral response in the polychaete Hydroides elegans. Microb Ecol 54:384–392

    PubMed  CAS  Google Scholar 

  • Huggett MJ, Williamson JE, de Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619

    PubMed  Google Scholar 

  • Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z (2004) A review of the impact of parasitic copepods on marine aquaculture. Zool Stud 43(2):229–243

    Google Scholar 

  • Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P, Camara M (2002) Cell-to-cell communication across the prokaryote–eukaryote boundary. Science 298:1207

    PubMed  Google Scholar 

  • Joint I, Tait K, Wheeler G (2007) Cross-kingdom signaling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos T R Soc B 362:1223–1233

    CAS  Google Scholar 

  • Kastbjerg VG, Nielsen KF, Dalsgaard I, Rasch M, Bruhn JB, Givskov M, Gram L (2007) Profiling acylated homoserine lactones in Yersinia ruckeri and influence of exogenous acyl homoserine lactones and known quorum-sensing inhibitors on protease production. J Appl Microbiol 102:363–374

    PubMed  CAS  Google Scholar 

  • Kellam SJ, Walker JM (1989) Antibacterial activity from marine algae in laboratory culture. Eur J Phycol 24:191–194

    Google Scholar 

  • Kim SY, Lee SE, Kim YR, Kim CM, Ryu PY, Choy HE, Chung SS, Rhee JH (2003) Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48:1647–1664

    PubMed  CAS  Google Scholar 

  • Kim JS, Kim YH, Seo YW, Park S (2007) Quorum sensing inhibitors from the red alga, Ahnfeltiopsis flabelliformis. Biotechnol Bioproc E 12:308–311

    CAS  Google Scholar 

  • Kjelleberg S, Steinberg P (2001) Defences against bacterial colonisation of marine plants. In: Lindow SE, Hect-Poinar E, Elliot V (eds) Phyllosphere microbiology. APS, Minnesota, pp 157–172

    Google Scholar 

  • Lau SCK, Thiyagarajan V, Cheung SCK, Qian P-Y (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat Microb Ecol 38:41–51

    Google Scholar 

  • Leadbetter JR, Greenberg EP (2000) Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J Bacteriol 182(24):6921–6926

    PubMed  CAS  Google Scholar 

  • Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK (2002) Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 68:3919–3924

    PubMed  CAS  Google Scholar 

  • Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69–82

    PubMed  CAS  Google Scholar 

  • Lilley B, Bassler BL (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and σ-54. Mol Microbol 36:940–954

    CAS  Google Scholar 

  • Lynch MJ, Swift S, Kirke DF, Keevil CW, Dood CER, Williams P (2002) The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ Microbiol 4:18–28

    PubMed  CAS  Google Scholar 

  • Manefield M, de Nys R, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology+ 145:283–291

    PubMed  CAS  Google Scholar 

  • Manefield M, Harris L, Rice SA, de Nys R, Kjelleberg S (2000) Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl Environ Microbiol 66(5):2079–2084

    PubMed  CAS  Google Scholar 

  • Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology+ 148:1119–1127

    PubMed  CAS  Google Scholar 

  • Maximillen R, de Nys R, Holmström C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233–246

    Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    PubMed  CAS  Google Scholar 

  • Milton DL (2006) Quorum sensing in vibrios: complexity for diversification. Int J Med Microbiol 296:61–71

    PubMed  CAS  Google Scholar 

  • Milton DL, O’Toole R, Hörstedt P, Wolf-Watz H (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178(5):1310–1319

    PubMed  CAS  Google Scholar 

  • Milton DL, Hardman A, Camara M, Chhabra SR, Bycroft BW, Stewart GSAB, Williams P (1997) Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-l-homoserine lactone. J Bacteriol 179:3004–3012

    PubMed  CAS  Google Scholar 

  • Milton DL, Chalker VJ, Kirke D, Hardman A, Camara M, Williams P (2001) The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl) homeserine lactone and N-hexanoylhomeserine lactone. J Bacteriol 183:3537–3547

    PubMed  CAS  Google Scholar 

  • Mok KC, Wingreen NS, Bassler BL (2003) Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22:870–881

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Morohoshi T, Ebata A, Nakazawa S, Kato N, Ikeda T (2005) N-Acyl homoserine lactone-producing or -degrading bacteria isolated from the intestinal microbial flora of Ayu fish (Plecoglossus altivelis). Microbes Environ 20(4):264–268

    Google Scholar 

  • Morohoshi T, Nakazawa S, Ebata A, Kato N, Ikeda T (2008) Identification and characterization of N-acylhomoserine lactone-acylase from the fish intestinal Shewanella sp. strain MIB015. Biosci Biotech Bioch 72(7):1887–1893

    CAS  Google Scholar 

  • Muller-Feuga A (2000) The role of micro-algae in aquaculture: situation and trends. J Appl Phycol 12:527–534

    Google Scholar 

  • Muroga K (2001) Viral and bacterial diseases of marine fish and shellfish in Japanese hatcheries. Aquaculture 202:23–44

    Google Scholar 

  • Murray AG, Peeler EJ (2005) A framework for understanding the potential for emerging diseases in aquaculture. Prev Vet Med 67:223–235

    PubMed  Google Scholar 

  • Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518

    PubMed  CAS  Google Scholar 

  • Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322

    PubMed  CAS  Google Scholar 

  • Nelson EJ, Tunsjø HS, Fidopiastis PM, Sørum H, Ruby EG (2007) A novel lux operon in the crytptically bioluminescent fish pathogen Vibrio salmonicida is associated with virulence. Appl Environ Microbiol 73(6):1825–1833

    PubMed  CAS  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern aquaculture. Aquaculture 231:361–391

    Google Scholar 

  • Ni N, Li M, Wang J, Wong B (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29(1):65–124

    PubMed  CAS  Google Scholar 

  • Nyholm SV, McFall-Ngai MJ (1998) Sampling the microenvironment of the Euprymna scolopes light organ: description of a population of host cells with the bacterial symbiont Vibrio fischeri. Biol Bull 195:89–97

    PubMed  CAS  Google Scholar 

  • Nylund GM, Cervin G, Hermansson M, Pavia H (2005) Chemical inhibition of bacterial colonization by the red algae Bonnemaisonia hamifera. Mar Ecol Prog Ser 302:27–36

    CAS  Google Scholar 

  • Ohtani K, Hayashi H, Shimizu T (2002) The luxS gene is involved in cell–cell signaling for toxin production in Clostridium perfringens. Mol Microbiol 44:171–179

    PubMed  CAS  Google Scholar 

  • Padilla D, Real F, Gómez SE, Acosta B, Déniz S, Acosta F (2005) Virulence factors and pathogenicity of Hafnia alvei for gilthead seabream, Sparus aurata L. J Fish Dis 28:411–417

    PubMed  CAS  Google Scholar 

  • Palmer PJ, Burke MJ, Palmer CJ, Burke JB (2007) Developments in controlled green-water larval culture technologies for estuarine fishes in Queensland, Australia and elsewhere. Aquaculture 272:1–21

    Google Scholar 

  • Peters L, Konig GM, Wright AD, Pukall R, Stackebrandt E, Eberl L, Riedel K (2003) Secondary metabolites of Flustra foliacea and their influence on bacteria. Appl Environ Microbiol 69:3469–3475

    PubMed  CAS  Google Scholar 

  • Planas M, Cunha I (1999) Larviculture of marine fish: problems and perspectives. Aquaculture 177:171–190

    Google Scholar 

  • Rajamani S, Bauer WD, Robinson JB III, Farrow JM, Pesci EC, Teplitski M, Gao M, Sayre RT, Phillips DA (2008) The vitamin riboflavin and its derivative lumichrome activate the LasR bacterial quorum-sensing receptor. Mol Plant Microbe Int 21(9):1184–1192

    CAS  Google Scholar 

  • Rasch M, Buch C, Austin B, Slierendrecht WJ, Ekmann KS, Larsen JL, Johansen C, Riedel K, Eberl L, Givskov M, Gram L (2004) An inhibitor of bacterial quorum sensing reduces mortalities caused by vibriosis in rainbow trout (Onchorhynchus mykiss, Walbaum). Syst Appl Microbiol 27:350–359

    PubMed  CAS  Google Scholar 

  • Rasch M, Kastbjerg VG, Bruhn JB, Dalsgaard I, Givskov M, Gram L (2007) Quorum sensing signals are produced by Aeromonas salmonicida and quorum sensing inhibitors can reduce production of a potential virulence factor. Dis Aquat Organ 78:105–113

    PubMed  Google Scholar 

  • Rasmussen TB, Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296:149–161

    PubMed  CAS  Google Scholar 

  • Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christopherse C, Steinberg P, Kjelleberg S, Givskov M (2000) How Delisa pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology+ 146:3237–3244

    PubMed  CAS  Google Scholar 

  • Rasmussen TB, Bjarnsholt BT, Skindersoe ME, Hentzer M, Kristoffersen P, Kote M, Nielsen J, Eberl L, Givskov M (2005) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814

    PubMed  CAS  Google Scholar 

  • Redfield RJ (2002) Is quorum sensing a side of diffusion sensing. Trends Microbiol 10(8):365–370

    PubMed  CAS  Google Scholar 

  • Reitan KI, Rainuzzo JR, Øie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–221

    Google Scholar 

  • Ren D, Sims J, Wood TK (2001) Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. Environ Microbiol 3:731–736

    PubMed  CAS  Google Scholar 

  • Roque A, Molina-Aja A, Bolán-Mejía C, Gomez-Gil B (2001) In vitro susceptibility to 15 antibiotics of vibrios isolated from penaeid shrimps in Northwestern Mexico. Int J Antimicrob Ag 17:383–387

    CAS  Google Scholar 

  • Sayre R, Rajamani S, Teplitski M, Bauer W (2006) Bacterial quorum-sensing interference by Chlamydomonas reinhardtii. J Phycol 42:20–21

    Google Scholar 

  • Schaefer LA, Val DL, Hanzelka BL, Cronan JE Jr, Greenberg EP (1996) Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. PNAS 93(18):9505–9509

    PubMed  CAS  Google Scholar 

  • Schauder S, Bassler BL (2001) The languages of bacteria. Genes Dev 15:1468–1480

    PubMed  CAS  Google Scholar 

  • Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, de Nys R, Givskov (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol 10:56–63

    PubMed  CAS  Google Scholar 

  • Sommerset I, Krossøy B, Biering E, Frost P (2005) Vaccines for fish in aquaculture. Expert Rev Vaccin 4(1):89–101

    CAS  Google Scholar 

  • Subasinghe RP, Barg U, Tacon A (2000) Chemicals in Asian aquaculture: need, usage, issues and challenges. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of chemicals in aquaculture in Asia. Proceedings of the Meeting on the Use of Chemicals in Aquaculture in Asia, 20–22 May 1996, Tigbauan, Iloilo, Philippines, Southeast Asian Fisheries Development Center (SEAFDEC), Tigbauan, Iloilo, Philippines. 235 pp

  • Sultan Z, Miyoshi S-I, Shinoda S (2006) Presence of LuxS/AI-2 based quorum-sensing system in Vibrio mimicus: LuxO controls protease activity. Microbiol Immunol 50(5):407–417

    PubMed  CAS  Google Scholar 

  • Sun J, Daniel R, Wagner-Döbler I, Zeng A-P (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4:36

    PubMed  Google Scholar 

  • Swift S, Karylyshev 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  CAS  Google Scholar 

  • Swift S, Lynch MJ, Fish L, Kirke DF, Tomas JM, Stewart GSAB, William P (1999) Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect Immun 67:5192–5199

    PubMed  CAS  Google Scholar 

  • Tait K, Joint I, Daykin M, Milton DL, Williams P, Camara M (2005) Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol 7(2):229–240

    PubMed  CAS  Google Scholar 

  • Teasdale ME, Liu J, Wallace J, Akhlaghi F, Rowley DC (2009) Secondary metabolites produced by the marine bacterium Halobacillus salinus that inhibit quorum sensing-controlled phenotypes in Gram-negative bacteria. Appl Environ Microbiol 75:567–572

    PubMed  CAS  Google Scholar 

  • Tendencia EA, dela Peňa LD (2001) Antibiotic resistance of bacteria from shrimp ponds. Aquaculture 195:193–204

    CAS  Google Scholar 

  • Teplitski M, Chen H, Rajamani S, Gao M, Merighi M, Sayre RT, Robinson JB, Rolfe BG, Bauer WD (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interference with quorum sensing regulation in bacteria. Plant Physiol 134:137–146

    PubMed  CAS  Google Scholar 

  • Tinh NTN, Lin ND, Wood TK, Dierckens K, Sorgeloos P, Bossier P (2007a) Interference with the quorum sensing systems in a Vibrio harveyi strain alters the growth rate of gnotobiotically cultured rotifer Brachionus plicatilis. J Appl Microbiol 103:194–203

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Tinh NTN, Dierckens K, Sorgeloos P, Bossier P (2008b) A review of the functionality of probiotics in the larviculture food chain. Mar Biotechnol 10:1–12

    CAS  Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol R 64(4):655–671

    CAS  Google Scholar 

  • Visick KL, McFall-Ngai MJ (2000) An exclusive contract: specificity in the Vibrio fischeri–Euprymna scolopes partnership. J Bacteriol 182(7):1779–1787

    PubMed  CAS  Google Scholar 

  • Wang Q, Liu Q, Ma Y, Rui H, Zhang Y (2007) LuxO controls extracellular protease, haemolytic activities and siderophore production in fish pathogen Vibrio alginolyticus. J Appl Microbiol 103(5):1525–1534

    Google Scholar 

  • Wang L-H, Weng L-X, Dong Y-H, Zhang L-H (2004) Specificity and enzyme kinetics of the quorum-quenching N-acyl homoserine lactone lactonase (AHL-lactonase). J Biol Chem 279:13645–13651

    PubMed  CAS  Google Scholar 

  • Wang L-H, Dong Y-H, Zhang L-H (2008) Quorum quenching: impact and mechanisms. In: Winans SC, Bassler BL (eds) Chemical communication among bacteria. ASM, Washington, pp 379–392

    Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    PubMed  CAS  Google Scholar 

  • Weinberger F, Beltran J, Correa JA, Lion U, Pohnert G, Kumar N, Steinberg P, Kloareg B, Potin P (2007) Spore release in Acrochaetium sp. (Rhodophyta) is bacterially controlled. J Phycol 43:235–241

    Google Scholar 

  • Wheeler GL, Tait K, Taylor A, Brownlee C, Joint I (2006) Acyl-homoserine lactones modulate the settlement of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Environ 29:608–616

    PubMed  CAS  Google Scholar 

  • Williams P, Winzer K, Chan WC, Cámara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Phil Transac R Soc B 362:1119–1134

    CAS  Google Scholar 

  • Xavier KB, Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191–197

    PubMed  CAS  Google Scholar 

  • Xuan L, Han Y, Yang Q, Zhang X-H (2010) Detection of quorum sensing signal molecules and mutation of luxS gene in Vibrio ichthyoenteri. Res Microbiol 161(1):51–57

    Google Scholar 

  • Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Cámara M, Smith H, Williams P (2002) N-Acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70:5635–5646

    PubMed  CAS  Google Scholar 

  • Ye J, Ma Y, Liu Q, Zhao DL, Wang QY, Zhang YX (2008) Regulation of Vibrio alginolyticus virulence by the LuxS quorum-sensing system. J Fish Dis 31:161–169

    PubMed  CAS  Google Scholar 

  • You J, Xue X, Cao L, Lu X, Wang J, Zhang L, Zhou S (2007) Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Appl Microb Cell Physiol 76:1137–1144

    CAS  Google Scholar 

  • Zang T, Lee BWK, Cannon LM, Ritter KA, Dai S, Ren D, Wood TK, Zhou ZS (2009) A naturally occurring brominated furanone covalently modifies and inactivates LuxS. Bioorgan Med Chem Lett 19(21):6200–6204

    CAS  Google Scholar 

  • Zhang X-H, Austin B (2000) Pathogenicity of Vibrio harveyi to salmonids. J Fish Dis 23(2):93–102

    Google Scholar 

  • Zhao B, Zhang S, Qian P-Y (2003) Larval settlement of the silver- or goldlip pearl oyster Pinctada maxima (Jameson) in response to natural biofilms and chemical cues. Aquaculture 220:883–901

    Google Scholar 

Download references

Acknowledgments

The first author acknowledges financial supports from University Putra Malaysia (UPM) and the Malaysian Ministry of Higher Education (MOHE) through a doctoral grant. Tom Defoirdt is a postdoctoral fellow of FWO-Vlaanderen This work is supported by project no. G049108N granted by FWOVlaanderen.

Author information

Authors and Affiliations

  1. Laboratory of Aquaculture and Artemia Reference Center, Ghent University, Rozier 44, 9000, Ghent, Belgium

    F. M. I. Natrah, Tom Defoirdt, Patrick Sorgeloos & Peter Bossier

  2. Department of Aquaculture, Faculty of Agriculture, University Putra Malaysia, 43400, Serdang, Selangor, Malaysia

    F. M. I. Natrah

Authors
  1. F. M. I. Natrah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tom Defoirdt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick Sorgeloos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter Bossier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Bossier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Natrah, F.M.I., Defoirdt, T., Sorgeloos, P. et al. Disruption of Bacterial Cell-to-Cell Communication by Marine Organisms and its Relevance to Aquaculture. Mar Biotechnol 13, 109–126 (2011). https://doi.org/10.1007/s10126-010-9346-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-010-9346-3

Keywords

Search

Navigation