Skip to main content

Advertisement

SpringerLink
Log in

AiiA lactonase disrupts N-acylhomoserine lactone and attenuates quorum-sensing-related virulence in Pectobacterium carotovorum EMPCC

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Enzymatic degradation of N-acyl homoserine lactone (NAHL) was found to interfere with the quorum sensing (QS) system and related functions in several soil bacteria. In this research, the NAHL lactonase gene aiiA was amplified using aiiA-7F/aiiA7R PCR primers from the quorum sensing inhibitor rhizobacterium Bacillus sp. strain DMS133, and cloned. The plasmid pME7075, carrying the DMS133 aiiA gene under the constitutive lac promoter, was introduced into the plant pathogen Pectobacterium carotovorum EMPCC, creating strain EMPCC/aiiA. Heterologous expression of the DMS133 aiiA gene in EMPCC severely reduced the accumulation of the NAHL throughout growth, and completely prevented pigmentation of the CV026 bioreporter strain. Virulence analysis revealed that the P. carotovorum strain EMPCC/aiiA expressing AiiA lactonase had drastically reduced tissue maceration activity compared with the wild type EMPCC strain. These results provide evidence that AiiA plays an important role in the quorum quenching ability of Bacillus sp. DMS133 whose AHL degradation capacity was investigated previously. In addition, the communication signal-inactivation approach represents a promising strategy for the prevention of diseases in which virulence is regulated by QS signal molecules.

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

Similar content being viewed by others

References

  • Andersson RA, Eriksson AR, Heikinheimo R, Mae A, Pirhonen M, Koiv V, Hyytiäinen H, Tuikkala A, Palva ET (2000) Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR (Ecc). Mol Plant Microbe Interact 13:384–393

    Article  PubMed  CAS  Google Scholar 

  • Barnard AM, Salmond GP (2007) Quorum sensing in Erwinia species. Anal Bioanal Chem 387:415–423

    Article  PubMed  CAS  Google Scholar 

  • Barras F, Gijsegem F, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32:201–234

    Article  CAS  Google Scholar 

  • Cirou A, Uroz S, Chapelle E, Latour NO, Faure D, Dessaux Y (2009) Quorum sensing as a target for novel biocontrol strategies directed at Pectobacterium. Recent Develop Manag Plant Dis 1:121–131

    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 

  • 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 

  • Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468

    Article  PubMed  CAS  Google Scholar 

  • Jafra S, Przysowa J, Czajkowski R, Michta A, Garbeva P, Vander Wolf JM (2006) Detection and characterization of bacteria from the potato rhizosphere degrading N-acyl-homoserine lactone. Can J Microbiol 52:1006–1015

    Article  PubMed  CAS  Google Scholar 

  • Jones S, Yu B, Bainton NJ, Birdsall M, Bycroft BW, Chhabra SR, Cox AJ, Golby P, Reeves PJ, Stephens S, Winson MK, Salmond GPC, Stewart GSAB, Williams P (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12:2477–2482

    PubMed  CAS  Google Scholar 

  • Lamb JR, Patel H, Montminy T, Wagner VE, Iglewski BH (2003) Functional domains of the RhlR transcriptional regulator of Pseudomonas aeruginosa. J Bacteriol 185:7129–7139

    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 

  • Mahmoudi E, Sayed-Tabatabaei BE, Venturi V (2011) Virulence attenuation of pectobacterium carotovorum using N-Acyl-homoserine lactone degrading bacteria isolated from potato rhizosphere. Plant Pathol J 27:242–248

    Article  CAS  Google Scholar 

  • Manzano M, Cocolin L, Cantoni C, Comi G (2003) Bacillus cereus, Bacillus thuringiensis and Bacillus mycoides differentiation using a PCR-RE technique. Int J Food Microbiol 81:249–254

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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(9):3206–3213

    Article  PubMed  CAS  Google Scholar 

  • Muller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum- sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67(3):468–478

    Article  PubMed  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, Hass 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 

  • Sambrook J, Fritsch EF, Maniatis T (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, p 876

    Google Scholar 

  • Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Cámara M, Williams P, Quax WJ (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74(3):1673–1682

    Article  PubMed  CAS  Google Scholar 

  • Toth IK, Birch PR (2005) Rotting softly and stealthily. Curr Opin Plant Biol 8:424–429

    Article  PubMed  CAS  Google Scholar 

  • Ulrich RL (2004) Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Appl Environ Microbiol 70(10):6173–6180

    Article  PubMed  CAS  Google Scholar 

  • Uroz S, Dessaux Y, Oger P (2009) Qourum sensing and Qourum quenching: the Yin and Yang of bacterial communicatio. Chembiochem 10:205–216

    Article  PubMed  CAS  Google Scholar 

  • Venturi V (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30:274–291

    Article  PubMed  CAS  Google Scholar 

  • Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404

    Article  PubMed  CAS  Google Scholar 

  • Wopperer J, Cardona ST, Huber B, Jacobi CA, Valvano MA, Eberl L (2006) A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl Environ Microbiol 72(2):1579–1587

    Article  PubMed  CAS  Google Scholar 

  • Zheng HM, Zhong ZT, Lai X, Chen WX, Li SP, Zhu J (2006) A LuxR/LuxItype quorum sensing system in a plant bacterium, Mesorhizobium tianshanense, controls symbiotic nodulation. J Bacteriol 188:1943–1949

    Article  PubMed  CAS  Google Scholar 

  • Zhu CG, Yu ZN, Sun M (2006) Restraining Erwinia virulence by expression of Nacyl homoserine lactonase gene pro3A-aiiA in Bacillus thuringiensis subsp. leesis. Biotechnol Bioeng 95:526–532

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by a research grant (project no. 1390424-411) from the Research Council of the Khorasgan Branch, Islamic Azad University of Iran. The Authors are grateful to Ms. Leila Mirshafi for critical editing of the manuscript.

Author information

Authors and Affiliations

  1. Young Researcher’s Club, Khorasgan Branch, Islamic Azad University, PO BOX 81595-158, Isfahan, Iran

    Esmaeil Mahmoudi & Davood Naderi

  2. Plant Bacteriology Group, International Center for Genetic Engineering and Biotechnology, Padriciano, Trieste, Italy

    Vittorio Venturi

Authors
  1. Esmaeil Mahmoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Davood Naderi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vittorio Venturi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Esmaeil Mahmoudi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mahmoudi, E., Naderi, D. & Venturi, V. AiiA lactonase disrupts N-acylhomoserine lactone and attenuates quorum-sensing-related virulence in Pectobacterium carotovorum EMPCC. Ann Microbiol 63, 691–697 (2013). https://doi.org/10.1007/s13213-012-0521-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-012-0521-9

Keywords

Search

Navigation