Skip to main content
SpringerLink
Log in

N-acyl homoserine lactones are degraded via an amidolytic activity in Comamonas sp. strain D1

  • Short Communication
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abtsract

Comamonas strain D1 enzymatically inactivates quorum-sensing (QS) signal molecules of the N-acyl homoserine lactone (N-AHSL) family, and exhibits the broadest inactivation range of known bacteria. It degrades N-AHSL with acyl-side chains ranging from 4 to 16 carbons, with or without 3-oxo or 3-hydroxy substitutions. N-AHSL degradation yields HSL but not N-acyl homoserine: strain D1 therefore harbors an amidohydrolase activity. Strain D1 is the fifth bacterium species in which an N-AHSL amidohydrolase is described. Consistent with its N-AHSL degradation ability, strain D1 efficiently quenches various QS-dependent functions in other bacteria, such as violacein production by Chromobacterium violaceum and pathogenicity and antibiotic production in Pectobacterium.

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

References

  • Bainton NJ, Stead P, Chhabra SR, Bycroft BW, Salmond GP, Stewart GS, Williams P (1992) N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem J 288:997–1004

    PubMed  CAS  Google Scholar 

  • Carlier A, Uroz S, Smadja B, Fray R, Latour X, Dessaux Y, Faure D (2003) The Ti plasmid of Agrobacterium tumefaciens harbors an attM paralogous gene aiiB also encoding N-acylhomoserine lactonase activity. Appl Environ Microbiol 69:4989–4993

    Article  PubMed  CAS  Google Scholar 

  • Carlier A, Chevrot R, Dessaux Y, Faure D (2004) The assimilation of gamma-butyrolactone in agrobacterium tumefaciens C58 interferes with the accumulation of the N-acyl-homoserine lactone signal. Mol Plant Microbe Interact 17:951–957

    PubMed  CAS  Google Scholar 

  • Castang S, Chantegrel B, Deshayes C, Dolmazon R, Gouet P, Haser R, Reverchon S, Nasser W, Hugouvieux-Cotte-Pattat N, Doutheau A (2004) N-Sulfonyl homoserine lactones as antagonists of bacterial quorum sensing. Bioorg Med Chem Lett 14:5145–5149

    Article  PubMed  CAS  Google Scholar 

  • Chhabra SR, Stead P, Bainton NJ, Salmond GP, Stewart GS, Williams P, Bycroft BW (1993) Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl)-L-homoserine lactone. J Antibiot (Tokyo) 46:441–454

    CAS  Google Scholar 

  • Chhabra SR, Harty C, Hooi DS, Daykin M, Williams P, Telford G, Pritchard DI, Bycroft BW (2003) Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-L-homoserine lactone as immune modulators. J Med Chem 46:97–104

    Article  PubMed  CAS  Google Scholar 

  • Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97:3526–3531

    Article  PubMed  CAS  Google Scholar 

  • Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Huang JJ, Han JI, Zhang LZ, Leadbetter JR (2003) Utilization of acyl-Homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69:5941–5949

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Camara M, Chhabra SR, Hardie KR, Bycroft BW, Lazdunski A, Salmond GPC, Stewart GSAB, Williams P (1998) In vitro biosynthesis of the Pseudomonas aeruginosa quorum-sensing signal molecule N-butanoyl-L-homoserine lactone. Mol Microbiol 28:193–203

    Article  PubMed  CAS  Google Scholar 

  • Kang BR, Lee JH, Ko SJ, Lee YH, Cha JS, Cho BH, Kim YC (2004) Degradation of acyl-homoserine lactone molecules by acinetobacter sp strain C1010. Can J Microbiol 50:935–941

    Article  PubMed  CAS  Google Scholar 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Lin YH, Xu JL, Hu J, Wang LH, Ong SL, Leadbetter JR, Zhang LH (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47:849–860

    Article  PubMed  Google Scholar 

  • Luo ZQ, Su S, Farrand SK (2003) In situ activation of the quorum-sensing transcription factor TraR by cognate and noncognate acyl-homoserine lactone ligands: kinetics and consequences. J Bacteriol 185:5665–5672

    Article  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 (N-AHSL)-mediated gene expression by displacing the N-AHSL signal from its receptor protein. Microbiology 145:283–291

    PubMed  CAS  Google Scholar 

  • McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GS, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703–3711

    Article  PubMed  CAS  Google Scholar 

  • Olsen JA, Severinsen R, Rasmussen TB, Hentzer M, Givskov M, Nielsen J (2002) Synthesis of new 3- and 4-substituted analogues of acyl homoserine lactone quorum sensing autoinducers. Bioorg Med Chem Lett 12:325–328

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Lee SJ, Oh TK, Oh JW, Koo BT, Yum DY, Lee JK (2003) AhlD an N-acylhomoserine lactonase in Arthrobacter sp and predicted homologues in other bacteria. Microbiology 149:1541–1550

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY (2005) Identification of extracellular N-Acylhomoserine lactone acylase from a Streptomyces sp and its application to quorum quenching. Appl Environ Microbiol 71:2632–2641

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Hwang BJ, Shin MH, Kim JA, Kim HK, Lee JK (2006) N-acylhomoserine lactonase producing Rhodococcus spp with different AHL-degrading activities. FEMS Microbiol Lett 261:102–108

    Article  PubMed  CAS  Google Scholar 

  • Persson T, Hansen TH, Rasmussen TB, Skinderso ME, Givskov M, Nielsen J (2005) Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3:253–62

    Article  PubMed  CAS  Google Scholar 

  • Peters L, König 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen TB, Givskov M (2006).Quorum sensing inhibitors: a bargain of effects. Microbiology 152:895–904

    Article  PubMed  CAS  Google Scholar 

  • Reimmann C, Ginet N, Michel L, Keel C, Michaux P, Krishnapillai V, Zala M, Heurlier K, Triandafillu K, Harms H, Defago G, Haas D (2002) Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148:923–932

    PubMed  CAS  Google Scholar 

  • Shaw PD, Ping G, Daly SL, Cha C, Cronan JE Jr, Rinehart KL, Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci USA 94:6036–6041

    Article  PubMed  CAS  Google Scholar 

  • Smith KM, Bu Y, Suga H (2003) Library screening for synthetic agonists and antagonists of a Pseudomonas aeruginosa autoinducer. Chem Biol 10:563–571

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648

    PubMed  CAS  Google Scholar 

  • Uroz S, Dangelo C, Carlier A, Faure D, Petit A, Oger P, Sicot C, Dessaux Y (2003) Novel bacteria degrading N-acyl homoserine lactones and their use as quenchers of quorum-sensing regulated functions of plant pathogenic bacteria. Microbiology 149:1981–1989

    Article  PubMed  CAS  Google Scholar 

  • Uroz S, Chhabra SR, Càmara M, Williams P, Oger PM, Dessaux Y (2005) N-acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151:3313–3322

    Article  PubMed  CAS  Google Scholar 

  • Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482

    Article  CAS  Google Scholar 

  • Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404

    Article  PubMed  CAS  Google Scholar 

  • Winans SC, Bassler BL (2002) Mob psychology. J Bacteriol 184:873–883

    Article  PubMed  CAS  Google Scholar 

  • Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GSAB (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acylhomoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163:185–192

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Song Z, Hentzer M, Andersen JB, Molin S, Givskov M, Hoiby N (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53:1054–1061

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang HB, Wang LH, Zhang LH (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 99:4638–4643

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was made possible by grants from the European Union Vth Framework Programme EcoSafe (QLK3-2000-01759) to P.W. and Y.D.; from the European Union Marie Curie programme (QLK1 1999 50 455) to P.W. and S.U. S.U. was also supported by a Fellowship from the French Ministère de la Recherche et de la Technologie, all of them being gratefully acknowledged. The authors also thank Chris Harty (Nottingham) for helpful discussions and comments on the manuscript, Mavis Daykin and Catherine Ortori (Nottingham) for HPLC and LC-MS/MS analysis, and Denis Faure (Gif-sur-Yvette) for his interest in, and helpful comments on this work.

Author information

Authors and Affiliations

  1. CNRS, ISV, Bâtiment 23, Avenue de la Terrasse, 91198, Gif-sur-Yvette, France

    Stéphane Uroz & Yves Dessaux

  2. Laboratoire de Sciences de la Terre, UMR5570 CNRS-ENS-UCBL, Ecole Normale Supérieure, 43 Allée D’Italie, 69364, Lyon CEDEX 07, France

    Phil Oger

  3. Institute of Infection, Immunity and Inflammation, Centre for Biomolecular Sciences, University of Nottingham, Nottingham, NG7 2RD, UK

    Siri Ram Chhabra, Miguel Cámara & Paul Williams

Authors
  1. Stéphane Uroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phil Oger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siri Ram Chhabra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Miguel Cámara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yves Dessaux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yves Dessaux.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uroz, S., Oger, P., Chhabra, S.R. et al. N-acyl homoserine lactones are degraded via an amidolytic activity in Comamonas sp. strain D1. Arch Microbiol 187, 249–256 (2007). https://doi.org/10.1007/s00203-006-0186-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-006-0186-5

Keywords

Search

Navigation