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The luxS Gene Is Involved in AI-2 Production, Pathogenicity, and Some Phenotypes in Erwinia amylovora

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Abstract

Erwinia amylovora causes fire blight of apple, pear, and other members of the Rosaceae family. The enzyme LuxS catalyzes the last step in the production of autoinducer-2 (AI-2), a molecule implicated with quorum sensing in many bacterial species. It is now well recognized that LuxS also plays a central role in sulfur metabolism and in the activated methyl cycle, which is responsible for the generation of S-adenosyl-l-methionine. A research paper has reported that luxS is not involved with quorum sensing in Er. amylovora, but in our study, Er. amylovora strain NCPPB1665 (Ea1665) produced luxS-dependent extracellular AI-2 activity. Additionally, the maximal AI-2 activity occurred during late-exponential and early-stationary growth phases and diminished during the stationary phase. The luxS mutant of Ea1665 was constructed, and the phenotypes of a defined luxS mutant have been characterized. Inactivation of luxS in Ea1665 impaired motility, extracellular polysaccharide (EPS) production, and tolerance for hydrogen peroxide, and reduced virulence on pear leaves.

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References

  1. Balestrino D, Haagensen JA, Rich C, Forestier C (2005) Characterization of type 2 quorum sensing in Klebsiella pneumoniae and relationship with biofilm formation. J Bacteriol 187:2870–2880

    Article  PubMed  CAS  Google Scholar 

  2. Bassler BL (1999) How bacteria talk to each other: Regulation of gene expression by quorum sensing. Curr Opin Microbiol 2:582–587

    Article  PubMed  CAS  Google Scholar 

  3. 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 

  4. Burgess NA, Kirke DF, Williams P et al (2002) LuxS-dependent quorum-sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence. Microbiology 148:763–772

    PubMed  CAS  Google Scholar 

  5. Burse A, Weingart H, Ullrich MS (2004) The phytoalexine-inducible multidrug efflux pump, AcrAB, contributes to virulence in the fire blight pathogen, Erwinia amylovora. Mol Plant-Microbe Interact 17:43–54

    Article  PubMed  CAS  Google Scholar 

  6. Chen X, Schauder S, Potier N et al (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549

    Article  PubMed  CAS  Google Scholar 

  7. Coulthurst SJ, Kathryn S, Lilley KS, Salmond GPC (2006) Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora. Mol Plant Pathol 7:31–45

    Article  CAS  Google Scholar 

  8. Dunny GM, Leonard BA (1997) Cell–cell communication in Gram-positive bacteria. Annu Rev Microbiol 51:527–564

    Article  PubMed  CAS  Google Scholar 

  9. Elvers KT, Park SF (2002) Quorum sensing in Campylobacter jejuni: detection of a luxS-encoded signaling molecule. Microbiology 148:1475–1481

    PubMed  CAS  Google Scholar 

  10. Fuqua C, Greenberg EP (1998) Self-perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1:183–189

    Article  PubMed  CAS  Google Scholar 

  11. Greenberg EP, Hastings JW, Ulitzer S (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87–91

    Article  CAS  Google Scholar 

  12. Johnson KB, Stockwell VO (1998) Management of fire blight: a case study in microbial ecology. Annu Rev Phytopathol 36:227–248

    Article  PubMed  CAS  Google Scholar 

  13. Jones MB, Blaser MJ (2003) Detection of a luxS-signaling molecule in Bacillus anthracis. Infect Immun 71:3914–3919

    Article  PubMed  CAS  Google Scholar 

  14. Joyce EA, Bassle BL, Wright A (2000) Evidence for a signaling system in Helicobacter pylori: detection of a luxS-encoded autoinducer. J Bacteriol 182:3638–3643

    Article  PubMed  CAS  Google Scholar 

  15. Kim SY, Lee SE, Kim YR et al (2003) Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system. Mol Microbiol 48:1647–1664

    Article  PubMed  CAS  Google Scholar 

  16. Laasik E, Andresen L, Mäe A (2006) Type II quorum sensing regulates virulence in Erwinia carotovora ssp. Carotovora. FEMS Microbiol Lett 258:227–234

    Article  PubMed  CAS  Google Scholar 

  17. Leigh JA, Coplin DL (1992) Exopolysaccharides in plant–bacterial interaction. Annu Rev Microbiol 46:307–346

    Article  PubMed  CAS  Google Scholar 

  18. Lyon WR, Madden JC, Levin JC et al (2001) Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42:145–157

    Article  PubMed  CAS  Google Scholar 

  19. Martinec T, Kocur M (1964) A taxonomic study of Erwinia amylovora (Burrill 1882) Winslow et al. 1920. Int Bull Bacteriol Nomencl Taxon 14:5–14

  20. Miller MB, Skorupski K, Lenz DH et al (2002) Parallel quorum-sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303–314

    Article  PubMed  CAS  Google Scholar 

  21. Mohammadi M, Geider K (2007) Autoinducer-2 of the fire blight pathogen Erwinia amylovora and other plant associated bacteria. FEMS Microbiol Lett 266:34–41

    Article  PubMed  CAS  Google Scholar 

  22. 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

    Article  PubMed  CAS  Google Scholar 

  23. Molina L, Rezzonico F, Défago G, Duffy B (2005) Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J Bacteriol 187:3206–3213

    Article  PubMed  CAS  Google Scholar 

  24. Nakahira Y, Katayama M, Miyashita H et al (2004) Global gene repression by KaiC as a master process of prokaryotic circadian system. PNAS 101:881–885

    Article  PubMed  CAS  Google Scholar 

  25. Novick RP, Muir TW (1999) Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. Curr Opin Microbiol 2:40–45

    Article  PubMed  CAS  Google Scholar 

  26. 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

    Article  PubMed  CAS  Google Scholar 

  27. Parsek MR, Greenberg EP (2000) Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci U S A 97:8789–8793

    Article  PubMed  CAS  Google Scholar 

  28. Rezzonico F, Duffy B (2007) The role of luxS in the fire blight pathogen Erwinia amylovora is limited to metabolism and does not involve quorum sensing. Molecular Plant–Microbe Interact 20:1284–1297

    Article  CAS  Google Scholar 

  29. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, NY

    Google Scholar 

  30. Schauder S, Shokat K, Surette MG, Bassler BL (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41:463–476

    Article  PubMed  CAS  Google Scholar 

  31. Schneider R, Lockatell CV, Johnson D, Belas R (2002) Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148:773–782

    PubMed  CAS  Google Scholar 

  32. Stroeher UH, Paton AW, Ogunniyi AD, Paton JC (2003) Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infect Immun 71:3206–3212

    Article  PubMed  CAS  Google Scholar 

  33. Surette MG, Bassler BL (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 95:7046–7050

    Article  PubMed  CAS  Google Scholar 

  34. Surette MG, Bassler BL (1999) Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 31:585–595

    Article  PubMed  CAS  Google Scholar 

  35. Vanneste JL (2000) Fire blight: the disease and its causative agent, Erwinia amylovora. CABI Publishing, Wallingford, Oxon, UK

    Google Scholar 

  36. Venisse JS, Barny MA, Paulin JP, Brisset MN (2003) Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS Lett 537:198–202

    Google Scholar 

  37. Venturi V, Venuti C, Devescovi G et al (2004) The plant pathogen Erwinia amylovora produces acyl-homoserine lactone signal molecules in vitro and in planta. FEMS Microbiol Lett 241:179–183

    Article  PubMed  CAS  Google Scholar 

  38. Williams P, Camara M, Hardman A et al (2000) Quorum sensing and the population-dependent control of virulence. Philos Trans R Soc Lond B Biol Sci 355:667–680

    Article  PubMed  CAS  Google Scholar 

  39. Winzer K, Sun YH, Green A et al (2002) Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection. Infect Immun 70:2245–2248

    Article  PubMed  CAS  Google Scholar 

  40. Withers H, Swift S, Williams P (2001) Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 4:186–193

    Article  PubMed  CAS  Google Scholar 

  41. Zhu J, Miller MB, Vance RE et al (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99:3129–3134

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Professor Bonnie L. Basle at Princeton University and Professor Zhang Le in China Plant Quarantine Experimental Institute for kindly providing Vibrio harveyi BB170 and Ea1665 respectively. We also thank Dr. Ron Walcott from the University of Georgia for critical revision of this article. This research was supported by the China National Basic Research and Development Project (2002CB111402) and the National Key Technologies Research and Development Program (2006BAD08A14).

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Authors and Affiliations

  1. College of Plant Protection, Key Laboratory of Monitoring and Management of Plant Diseases and Insects, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Yan Gao, Junxian Song, Baishi Hu, Lei Zhang, Qianqian Liu & Fengquan Liu

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  1. Yan Gao
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  2. Junxian Song
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  3. Baishi Hu
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Correspondence to Baishi Hu.

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Yan Gao and Junxian Song contributed equally to this research.

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Gao, Y., Song, J., Hu, B. et al. The luxS Gene Is Involved in AI-2 Production, Pathogenicity, and Some Phenotypes in Erwinia amylovora . Curr Microbiol 58, 1–10 (2009). https://doi.org/10.1007/s00284-008-9256-z

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  • DOI: https://doi.org/10.1007/s00284-008-9256-z

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