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Quenching quorum-sensing-dependent bacterial infection by anN-acyl homoserine lactonase
Naturevolume 411, pages813–817 (2001)Cite this article
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Abstract
Bacterial cells sense their population density through a sophisticated cell–cell communication system and trigger expression of particular genes when the density reaches a threshold. This type of gene regulation, which controls diverse biological functions including virulence, is known as quorum sensing1,2. Quorum-sensing signals, such as acyl-homoserine lactones (AHLs), are the essential components of the communication system. AHLs regulate virulence gene expression in a range of plant and animal (including human) bacterial pathogens3,4,5,6,7,8,9. AHL-producing tobacco restored the pathogenicity of an AHL-negative mutant ofErwinia carotovora10. Different bacterial species may produce different AHLs, which vary in the length and substitution of the acyl chain but contain the same homoserine lactone moiety. Here we show that the acyl-homoserine lactonase (AHL-lactonase), a new enzyme fromBacillus sp.11, inactivates AHL activity by hydrolysing the lactone bond of AHLs. Plants expressing AHL-lactonase quenched pathogen quorum-sensing signalling and showed significantly enhanced resistance toE.carotovora infection. Our results highlight a promising potential to use quorum-sensing signals as molecular targets for disease control, thereby broadening current approaches for prevention of bacterial infections.
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References
Fuqua, C., Winans, S. C. & Greenberg, E. P. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators.Annu. Rev. Microbiol.50, 727– 751 (1996).
Robson, N. D., Cox, A. R., McGowan, S. J., Bycroft, B. W. & Salmond, G. P. BacterialN-acyl-homoserine-lactone-dependent signaling and its potential biotechnological applications.Trends Biotechnol.15, 458– 464 (1997).
Jones, S. M. et al. TheLux autoinducer regulates the production of exoenzyme virulence determination inErwinia carotovora andPseudomonas aeruginosa.EMBO J.12, 2477– 2482 (1993).
Passador, L., Cook, J. M., Gambello, M. J., Rust, L. & Iglewski, B. H. Expression ofPseudomonas aeruginosa virulence genes requires cell-to-cell communication.Science260, 1127– 1130 (1993).
Pirhonen, M., Flego, D., Heikinheimo, R., & Palva, E. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogenErwinia carotovora.EMBO J.12, 2467– 2476 (1993).
von Bodman, S. B. & Farrand, S. K. Capsular polysaccharide biosynthesis and pathogenicity inErwinia stewartii require induction by anN-acylhomoserine lactone autoinducer.J. Bacteriol.177, 5000– 5008 (1995).
Costa, J. M. & Loper, J. E. EcbI and EcbR: homologs of LuxI and LuxR affecting antibiotic and exoenzyme production byErwinia carotovora subsp.betavasculorum.Can. J. Microbiol.43, 1164– 1171 (1997).
Dunphy, G., Miyamoto, C. & Meighen, E. A homoserine lactone autoinducer regulates virulence of an insect-pathogenic bacterium,Xenorhabdus nematophilus (Enterobacteriaceae).J. Bacteriol.179, 5288– 5291 (1997).
Lewenza, S., Conway, B., Greenberg, E. P. & Sokol, P. A. Quorum Sensing inBurkholderia cepacia: identification of the LuxRI Homologs CepRI.J. Bacteriol.181, 748– 756 (1999).
Fray, R. G. et al. Plants genetically modified to produceN-acylhomoserine lactones communicate with bacteria.Nature Biotech.17, 1017– 1020 (1999).
Dong, Y.-H., Xu, J.-L., Li, X.-C. & Zhang, L. H. AiiA, a novel enzyme inactivates acyl homoserine-lactone quorum-sensing signal and attenuates the virulence ofErwinia carotovora.Proc. Natl Acad. Sci. USA97, 3526– 3531 (2000).
von Bodman, S. B., Majerczak, D. R. & Coplin, D. L. A negative regulator mediates quorum-sensing control of exopolysaccharide production inPantoea stewartii subsp.stewartii.Proc. Natl Acad. Sci. USA95, 7687– 7692 (1998).
Welch, M. et al.N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity inErwinia.EMBO J.19, 631– 641 (2000).
Qin, Y. P. et al. Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm.EMBO J.19, 5212– 5221 (2000).
Pearson, J. P., Van Delden, C. & Iglewski, B. H. Active efflux and diffusion are involved in transport ofPseudomonas aeruginosa cell-to-cell signals.J. Bacteriol.181, 1203– 1210 (1999).
Zhu, J. & Winans, S. C. Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promotersin vitro and decreases TraR turnover rates in the whole cells.Proc. Natl Acad. Sci. USA96, 4832– 4837 (1999).
Leadbetter, J. R. & Greenberg, E. P. Metabolism of acyl-homoserine lactone quorum-sensing signals byVariovorax paradoxus.J. Bacteriol.182, 6921– 6926 (2000).
Pearson, J. P. et al. Structure of the autoinducer required for expression ofPseudomonas aeruginosa virulence genes.Proc. Natl Acad. Sci. USA91, 197– 201 (1994).
Winson, M. K. et al. MultipleN-acyl-l-homoserine lactones signal molecules regulate production of virulence determinants and secondary metabolites inPseudomonas aeruginosa.Proc. Natl Acad. Sci. USA92, 9427– 9431 (1995).
Zhang, L. H., Murphy, P. J., Kerr, A. & Tate, M. E.Agrobacterium conjugation and gene regulation byN-acyl-l-homoserine lactones.Nature362, 446– 447 (1993).
Gallois, P. & Marinho, P. inPlant Gene Transfer and Expression Protocols (ed. Jones, H.) 39– 48 (Humana, Totowa, New Jersey, 1995).
Beaujean, A., Sangwan, R. S., Lecardonnel, A. & Sangwan-Norreel, B. S.Agrobacterium-mediated transformation of three economically important potato cultivars using sliced internodal explants: an efficient protocol of transformation.J. Exp. Bot.49, 1589– 1595 (1998).
Borisjuk, N. V. et al. Calreticulin expression in plant cells: developmental regulation, tissue specificity and intracellular distribution.Planta206, 504– 514 (1998).
Givskov, M. et al. Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling.J. Bacteriol.178, 6618– 6622 (1996).
Manefield, M. et al. Evidence that halogenated furanones fromDelisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein.Microbiol.145, 283– 291 (1999).
Manefield, M., Harris, L., Rice, S. A., de Nys, R. & Kjelleberg, S. Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogenVibrio harveyi by intercellular signal antagonists.Appl. Environ. Microbiol.66, 2079– 2084 (2000).
Hoang, T. T. & Schweizer, H. P. Characterization ofPseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis.J. Bacteriol.181, 5489– 5497 (1999).
Borisjuk, N. V. et al. Production of recombinant proteins in plant root exudates.Nature Biotechnol.17, 466– 469 (1999).
Acknowledgements
We thank A. Kerr, M. E. Tate, V. Sundaresan and K. Sampath for critical reviews of the manuscript. Funding was provided by the National Science and Technology Board of Singapore.
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Yi-Hu Dong and Lian-Hui Wang: These authors contributed equally to this work
Lian-Hui Zhang: Correspondence and requests for materials should be addressed to L.-H.Z.
Authors and Affiliations
Laboratory of Biosignals and Bioengineering, Institute of Molecular Agrobiology, National University of Singapore, 1 Research Link, 117604, Singapore
Yi-Hu Dong, Lian-Hui Wang, Jin-Ling Xu, Hai-Bao Zhang, Xi-Fen Zhang & Lian-Hui Zhang
- Yi-Hu Dong
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- Jin-Ling Xu
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- Hai-Bao Zhang
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- Xi-Fen Zhang
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Dong, YH., Wang, LH., Xu, JL.et al. Quenching quorum-sensing-dependent bacterial infection by anN-acyl homoserine lactonase.Nature411, 813–817 (2001). https://doi.org/10.1038/35081101
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