1887

Abstract

Many bacteria harbour an incomplete quorum-sensing (QS) system, whereby they possess LuxR homologues without the QS acylhomoserine lactone (AHL) synthase, which is encoded by a homologue. An artificial AHL-producing plasmid was constructed using a gene encoding the C6-AHL [-hexanoyl homoserine lactone (HHL)] synthase from , and was introduced successfully into both the wild-type and a ( homologue) mutant of . Our data provide evidence to suggest that the PpoR–HHL complex, but neither PpoR nor HHL alone, could attenuate growth, antibiotic resistance and biofilm formation ability. In contrast, swimming motility, siderophore production and indole degradation were enhanced by PpoR–HHL. The addition of exogenous indole increased biofilm formation and reduced swimming motility. Interestingly, indole proved ineffective in the presence of PpoR–HHL, thereby suggesting that the PpoR–HHL complex masks the effects of indole. Our data were supported by transcriptome analyses, which showed that the presence of the plasmid-encoded AHL synthase altered the expression of many genes on the chromosome in strain KT2440. Our results showed that heterologous expression that occurs via horizontal gene transfer can regulate a broad range of specific target genes, resulting in alterations of the phenotype and physiology of host cells.

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2010-12-01
2019-10-15
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References

  1. Ahmer, B. M. ( 2004; ). Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 52, 933–945.[CrossRef]
    [Google Scholar]
  2. Alm, R. A. & Mattick, J. S. ( 1996; ). Identification of two genes with prepilin-like leader sequences involved in type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 178, 3809–3817.
    [Google Scholar]
  3. Barnhart, M. M. & Chapman, M. R. ( 2006; ). Curli biogenesis and function. Annu Rev Microbiol 60, 131–147.[CrossRef]
    [Google Scholar]
  4. Bertolla, F. & Simonet, P. ( 1999; ). Horizontal gene transfers in the environment: natural transformation as a putative process for gene transfers between transgenic plants and microorganisms. Res Microbiol 150, 375–384.[CrossRef]
    [Google Scholar]
  5. Case, R. J., Labbate, M. & Kjelleberg, S. ( 2008; ). AHL-driven quorum sensing circuits: their frequency and function among the proteobacteria. ISME J 2, 345–349.[CrossRef]
    [Google Scholar]
  6. Cha, C., Gao, P., Chen, Y. C., Shaw, P. D. & Farrand, S. K. ( 1998; ). Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria. Mol Plant Microbe Interact 11, 1119–1129.[CrossRef]
    [Google Scholar]
  7. Chandrakala, B., Shandil, R. K., Mehra, U., Ravishankar, S., Kaur, P., Usha, V., Joe, B. & de Sousa, S. M. ( 2004; ). High-throughput screen for inhibitors of transglycosylase and/or transpeptidase activities of Escherichia coli penicillin binding protein 1b. Antimicrob Agents Chemother 48, 30–40.[CrossRef]
    [Google Scholar]
  8. Chilton, M. D., Currier, T. C., Farrand, S. K., Bendich, A. J., Gordon, M. P. & Nester, E. W. ( 1974; ). Agrobacterium tumefaciens and PS8 bacteriophage DNA not detected in crown gall tumor DNA. Proc Natl Acad Sci U S A 71, 3672–3676.[CrossRef]
    [Google Scholar]
  9. Danhorn, T. & Fuqua, C. ( 2007; ). Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61, 401–422.[CrossRef]
    [Google Scholar]
  10. Davison, J. ( 1999; ). Genetic exchange between bacteria in the environment. Plasmid 42, 73–91.[CrossRef]
    [Google Scholar]
  11. Doronina, V. A. & Murray, N. E. ( 2001; ). The proteolytic control of restriction activity in Escherichia coli K-12. Mol Microbiol 39, 416–428.[CrossRef]
    [Google Scholar]
  12. Dunny, G. M. & Winans, S. C. ( 1999; ). Cell–Cell Signaling in Bacteria. Washington, DC. : American Society for Microbiology.
    [Google Scholar]
  13. Edgar, R. M., Domrachev, M. & Lash, A. E. ( 2002; ). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30, 207–210.[CrossRef]
    [Google Scholar]
  14. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. ( 1998; ). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95, 14863–14868.[CrossRef]
    [Google Scholar]
  15. Elasri, M., Delorme, S., Lemanceau, P., Stewart, G., Laue, B., Glickmann, E., Oger, P. M. & Dessaux, Y. ( 2001; ). Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp. Appl Environ Microbiol 67, 1198–1209.[CrossRef]
    [Google Scholar]
  16. Figurski, D. H. & Helinski, D. R. ( 1979; ). Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648–1652.[CrossRef]
    [Google Scholar]
  17. Fuqua, C. ( 2006; ). The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J Bacteriol 188, 3169–3171.[CrossRef]
    [Google Scholar]
  18. Fuqua, C. & Greenberg, E. P. ( 2002; ). Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3, 685–695.[CrossRef]
    [Google Scholar]
  19. Gao, R. & Stock, A. M. ( 2009; ). Biological insights from structures of two-component proteins. Annu Rev Microbiol 63, 133–154.[CrossRef]
    [Google Scholar]
  20. Hirakawa, H., Kodama, T., Takumi-Kobayashi, A., Honda, T. & Yamaguchi, A. ( 2009; ). Secreted indole serves as a signal for expression of type III secretion system translocators in enterohaemorrhagic Escherichia coli O157 : H7. Microbiology 155, 541–550.[CrossRef]
    [Google Scholar]
  21. Kang, Y. S. & Park, W. ( 2010; ). Contribution of quorum sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J Appl Microbiol, doi:.
    [Google Scholar]
  22. Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. ( 2007; ). A common mechanism of cellular death by bacterial antibiotics. Cell 130, 797–810.[CrossRef]
    [Google Scholar]
  23. Lairson, L. L., Henrissat, B., Davies, G. J. & Withers, S. G. ( 2008; ). Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77, 521–555.[CrossRef]
    [Google Scholar]
  24. Lawrence, J. G. ( 1997; ). Selfish operons and speciation by gene transfer. Trends Microbiol 5, 355–359.[CrossRef]
    [Google Scholar]
  25. Lee, J., Jayaraman, A. & Wood, T. K. ( 2007a; ). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7, 42.[CrossRef]
    [Google Scholar]
  26. Lee, Y., Yeom, J., Kang, Y. S., Kim, J., Sung, J. S., Jeon, C. O. & Park, W. ( 2007b; ). Molecular characterization of FprB (ferredoxin-NADP+ reductase) in Pseudomonas putida KT2440. J Microbiol Biotechnol 17, 1504–1512.
    [Google Scholar]
  27. Lee, Y., Kim, Y., Yeom, S., Kim, S., Park, S., Jeon, C. O. & Park, W. ( 2008; ). The role of disulfide bond isomerase A (DsbA) of Escherichia coli O157 : H7 in biofilm formation and virulence. FEMS Microbiol Lett 278, 213–222.[CrossRef]
    [Google Scholar]
  28. Lee, J., Maeda, T., Hong, S. H. & Wood, T. K. ( 2009a; ). Reconfiguring the quorum-sensing regulator SdiA of Escherichia coli to control biofilm formation via indole and N-acylhomoserine lactones. Appl Environ Microbiol 75, 1703–1716.[CrossRef]
    [Google Scholar]
  29. Lee, Y., Oh, S. & Park, W. ( 2009b; ). Inactivation of the Pseudomonas putida KT2440 dsbA gene promotes extracellular matrix production and biofilm formation. FEMS Microbiol Lett 297, 38–48.[CrossRef]
    [Google Scholar]
  30. Li, Y., Hao, G., Galvani, C. D., Meng, Y., De La Fuente, L., Hoch, H. C. & Burr, T. J. ( 2007; ). Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell–cell aggregation. Microbiology 153, 719–726.[CrossRef]
    [Google Scholar]
  31. Liu, H., Coulthurst, S. J., Pritchard, L., Hedley, P. E., Ravensdale, M., Humphris, S., Burr, T., Takle, G., Brurberg, M. B. & other authors ( 2008; ). Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4, e1000093.[CrossRef]
    [Google Scholar]
  32. Matilla, M. A., Ramos, J. L., Duque, E., de Dios Alché, J., Espinosa-Urgel, M. & Ramos-González, M. I. ( 2007; ). Temperature and pyoverdine-mediated iron acquisition control surface motility of Pseudomonas putida. Environ Microbiol 9, 1842–1850.[CrossRef]
    [Google Scholar]
  33. McClay, K., Boss, C., Keresztes, I. & Steffan, R. J. ( 2005; ). Mutations of toluene-4-monooxygenase that alter regiospecificity of indole oxidation and lead to production of novel indigoid pigments. Appl Environ Microbiol 71, 5476–5483.[CrossRef]
    [Google Scholar]
  34. McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S. & other authors ( 1997; ). Quorum sensing in Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143, 3703–3711.[CrossRef]
    [Google Scholar]
  35. Mohammadi, T., Karczmarek, A., Crouvoisier, M., Bouhss, A., Mengin-Lecreulx, D. & den Blaauwen, T. ( 2007; ). The essential peptidoglycan glycosyltransferase MurG forms a complex with proteins involved in lateral envelope growth as well as with proteins involved in cell division in Escherichia coli. Mol Microbiol 65, 1106–1121.[CrossRef]
    [Google Scholar]
  36. Mølbak, L., Licht, T. R., Kvist, T., Kroer, N. & Andersen, S. R. ( 2003; ). Plasmid transfer from Pseudomonas putida to the indigenous bacteria on alfalfa sprouts: characterization, direct quantification, and in situ location of transconjugant cells. Appl Environ Microbiol 69, 5536–5542.[CrossRef]
    [Google Scholar]
  37. Molina, M. A., Ramos, J. L. & Espinosa-Urgel, M. ( 2006; ). A two-partner secretion system is involved in seed and root colonization and iron uptake by Pseudomonas putida KT2440. Environ Microbiol 8, 639–647.[CrossRef]
    [Google Scholar]
  38. Nelson, K. E., Weinel, C., Paulsen, I. T., Dodson, R. J., Hilbert, H., Martins dos Santos, V. A., Fouts, D. E., Gill, S. R., Pop, M. & other authors ( 2002; ). Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4, 799–808.[CrossRef]
    [Google Scholar]
  39. Pontiroli, A., Simonet, P., Frostegard, A., Vogel, T. M. & Monier, J. M. ( 2007; ). Fate of transgenic plant DNA in the environment. Environ Biosafety Res 6, 15–35.[CrossRef]
    [Google Scholar]
  40. Rahmati, S., Yang, S., Davidson, A. L. & Zechiedrich, E. L. ( 2002; ). Control of the AcrAB multidrug efflux pump by quorum-sensing regulator SdiA. Mol Microbiol 43, 677–685.[CrossRef]
    [Google Scholar]
  41. Ramos-González, M. I., Campos, M. J. & Ramos, J. L. ( 2005; ). Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vivo expression technology capture and identification of root-activated promoters. J Bacteriol 187, 4033–4041.[CrossRef]
    [Google Scholar]
  42. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E., Jr, Rinehart, K. L. & Farrand, S. K. ( 1997; ). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94, 6036–6041.[CrossRef]
    [Google Scholar]
  43. Soulère, L., Frezza, M., Queneau, Y. & Doutheau, A. ( 2007; ). Exploring the active site of acyl homoserine lactones-dependent transcriptional regulators with bacterial quorum sensing modulators using molecular mechanics and docking studies. J Mol Graph Model 26, 581–590.[CrossRef]
    [Google Scholar]
  44. Subramoni, S. & Venturi, V. ( 2009a; ). LuxR-family ‘solos’: bachelor sensors/regulators of signalling molecules. Microbiology 155, 1377–1385.[CrossRef]
    [Google Scholar]
  45. Subramoni, S. & Venturi, V. ( 2009b; ). PpoR is a conserved unpaired LuxR solo of Pseudomonas putida which binds N-acyl homoserine lactones. BMC Microbiol 9, 125.[CrossRef]
    [Google Scholar]
  46. Venturi, V. ( 2006; ). Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30, 274–291.[CrossRef]
    [Google Scholar]
  47. Waters, C. M. & Bassler, B. L. ( 2005; ). Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21, 319–346.[CrossRef]
    [Google Scholar]
  48. Wei, B. L., Brun-Zinkernagel, A. M., Simecka, J. W., Pruss, B. M., Babitzke, P. & Romeo, T. ( 2001; ). Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40, 245–256.[CrossRef]
    [Google Scholar]
  49. Wood, T. K., González Barrios, A. F., Herzberg, M. & Lee, J. ( 2006; ). Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72, 361–367.[CrossRef]
    [Google Scholar]
  50. Xiao, R. & Kisaalita, W. ( 1998; ). Fluorescent pseudomonad pyoverdines bind and oxidize ferrous ion. Appl Environ Microbiol 64, 1472–1476.
    [Google Scholar]
  51. Yao, Y., Martinez-Yamout, M. A., Dickerson, T. J., Brogan, A. P., Wright, P. E. & Dyson, H. J. ( 2006; ). Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J Mol Biol 355, 262–273.[CrossRef]
    [Google Scholar]
  52. Yin, S., Fuangthong, M., Laratta, W. P. & Shapleigh, J. P. ( 2003; ). Use of a green fluorescent protein-based reporter fusion for detection of nitric oxide produced by denitrifiers. Appl Environ Microbiol 69, 3938–3944.[CrossRef]
    [Google Scholar]
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