1887

Abstract

Quorum sensing (QS)-dependent biofilm formation and motility were controlled by AqsR in DR1. QS-controlled phenotypes appeared to be inhibited by indole and the mutant had the same phenotypes. We demonstrated that the turnover rate of AqsR became more rapid without the -acylhomoserine lactone (AHL) signal, and that indole could increase the expression of many protease and chaperone proteins. The addition of exogenous indole decreased the expression of two AqsR-targeted genes: AOLE_03905 (putative surface adhesion protein) and AOLE_11355 (-asparaginase). The overexpression of AqsR in was impossible with the indole treatment. Surprisingly, our [S]methionine pulse-labelling data demonstrated that the stability and folding of AqsR protein decreased in the presence of indole without changing mRNA expression in . Interestingly, indole resulted in a loss of TraR-dependent expression in an indicator strain. However, when indole was added after incubation with exogenous AHL, indole could not inhibit the TraR-dependent expression of the promoter. This indicated that AHL-bound TraR could be protective against indole, but TraR without AHL could not be active in the presence of indole. Here, we provided evidence for the first time showing that the indole effect on QS-controlled bacterial phenotypes is due to inhibited QS regulator folding and not a reduced QS signal.

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2013-12-01
2024-03-28
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References

  1. Baldi F., Ivosevic N., Minacci A., Pepi M., Fani R., Svetlicic V., utic V.( 1999). Adhesion of Acinetobacter venetianus to diesel fuel droplets studied with in situ electrochemical and molecular probes. Appl Environ Microbiol 65:2041–2048[PubMed]
    [Google Scholar]
  2. Botsford J. L., Demoss R. D.( 1972). Escherichia coli tryptophanase in the enteric environment. J Bacteriol 109:74–80[PubMed]
    [Google Scholar]
  3. 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 [View Article][PubMed]
    [Google Scholar]
  4. Chai Y., Winans S. C.( 2009). The chaperone GroESL enhances the accumulation of soluble, active TraR protein, a quorum-sensing transcription factor from Agrobacterium tumefaciens. J Bacteriol 191:3706–3711 [View Article][PubMed]
    [Google Scholar]
  5. Chimerel C., Field C. M., Piñero-Fernandez S., Keyser U. F., Summers D. K.( 2012). Indole prevents Escherichia coli cell division by modulating membrane potential. Biochim Biophys Acta 1818:1590–1594 [View Article][PubMed]
    [Google Scholar]
  6. Chu W., Zere T. R., Weber M. M., Wood T. K., Whiteley M., Hidalgo-Romano B., Valenzuela E. Jr, McLean R. J.( 2012). Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl Environ Microbiol 78:411–419 [View Article][PubMed]
    [Google Scholar]
  7. Cohn M. T., Ingmer H., Mulholland F., Jørgensen K., Wells J. M., Brøndsted L.( 2007). Contribution of conserved ATP-dependent proteases of Campylobacter jejuni to stress tolerance and virulence. Appl Environ Microbiol 73:7803–7813 [View Article][PubMed]
    [Google Scholar]
  8. Costa E. D., Chai Y., Winans S. C.( 2012). The quorum-sensing protein TraR of Agrobacterium tumefaciens is susceptible to intrinsic and TraM-mediated proteolytic instability. Mol Microbiol 84:807–815 [View Article][PubMed]
    [Google Scholar]
  9. Duerkop B. A., Varga J., Chandler J. R., Peterson S. B., Herman J. P., Churchill M. E., Parsek M. R., Nierman W. C., Greenberg E. P.( 2009). Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191:3909–3918 [View Article][PubMed]
    [Google Scholar]
  10. Fuqua W. C., Winans S. C., Greenberg E. P.( 1994). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275[PubMed]
    [Google Scholar]
  11. Gaddy J. A., Actis L. A.( 2009). Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol 4:273–278 [View Article][PubMed]
    [Google Scholar]
  12. Gallagher L. A., McKnight S. L., Kuznetsova M. S., Pesci E. C., Manoil C.( 2002). Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472–6480 [View Article][PubMed]
    [Google Scholar]
  13. Gohl O., Friedrich A., Hoppert M., Averhoff B.( 2006). The thin pili of Acinetobacter sp. strain BD413 mediate adhesion to biotic and abiotic surfaces. Appl Environ Microbiol 72:1394–1401 [View Article][PubMed]
    [Google Scholar]
  14. González R. H., Dijkshoorn L., Van den Barselaar M., Nudel C.( 2009). Quorum sensing signal profile of Acinetobacter strains from nosocomial and environmental sources. Rev Argent Microbiol 41:73–78[PubMed]
    [Google Scholar]
  15. Han T. H., Lee J. H., Cho M. H., Wood T. K., Lee J.( 2011). Environmental factors affecting indole production in Escherichia coli. Res Microbiol 162:108–116 [View Article][PubMed]
    [Google Scholar]
  16. Helling R. B., Janes B. K., Kimball H., Tran T., Bundesmann M., Check P., Phelan D., Miller C.( 2002). Toxic waste disposal in Escherichia coli. J Bacteriol 184:3699–3703 [View Article][PubMed]
    [Google Scholar]
  17. Hentzer M., Wu H., Andersen J. B., Riedel K., Rasmussen T. B., Bagge N., Kumar N., Schembri M. A., Song Z.& other authors ( 2003). Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815 [View Article][PubMed]
    [Google Scholar]
  18. Jung J., Baek J.-H., Park W.( 2010). Complete genome sequence of the diesel-degrading Acinetobacter sp. strain DR1. J Bacteriol 192:4794–4795 [View Article][PubMed]
    [Google Scholar]
  19. Kang Y. S., Park W.( 2010a). Contribution of quorum-sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J Appl Microbiol 109:1650–1659[PubMed]
    [Google Scholar]
  20. Kang Y. S., Park W.( 2010b). Trade-off between antibiotic resistance and biological fitness in Acinetobacter sp. strain DR1. Environ Microbiol 12:1304–1318 [View Article][PubMed]
    [Google Scholar]
  21. Kang Y. S., Kim Y. J., Jeon C. O., Park W.( 2006). Characterization of naphthalene-degrading Pseudomonas species isolated from pollutant-contaminated sites: oxidative stress during their growth on naphthalene. J Microbiol Biotechnol 16:1819–1825
    [Google Scholar]
  22. Karlin D. A., Mastromarino A. J., Jones R. D., Stroehlein J. R., Lorentz O.( 1985). Fecal skatole and indole and breath methane and hydrogen in patients with large bowel polyps or cancer. J Cancer Res Clin Oncol 109:135–141 [View Article][PubMed]
    [Google Scholar]
  23. Kawamura-Sato K., Shibayama K., Horii T., Iimuma Y., Arakawa Y., Ohta M.( 1999). Role of multiple efflux pumps in Escherichia coli in indole expulsion. FEMS Microbiol Lett 179:345–352 [View Article][PubMed]
    [Google Scholar]
  24. Kim J., Park W.( 2013). Identification and characterization of genes regulated by AqsR, a LuxR-type regulator in Acinetobacter oleivorans DR1. Appl Microbiol Biotechnol 97:6967–6978 [View Article][PubMed]
    [Google Scholar]
  25. Kim Y. G., Lee J. H., Cho M. H., Lee J.( 2011). Indole and 3-indolylacetonitrile inhibit spore maturation in Paenibacillus alvei.. BMC Microbiol 11:119 [View Article][PubMed]
    [Google Scholar]
  26. Kim J., Hong H., Heo A., Park W.( 2013). Indole toxicity involves the inhibition of adenosine triphosphate production and protein folding in Pseudomonas putida. FEMS Microbiol Lett 343:89–99 [View Article][PubMed]
    [Google Scholar]
  27. Kobayashi A., Hirakawa H., Hirata T., Nishino K., Yamaguchi A.( 2006). Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J Bacteriol 188:5693–5703 [View Article][PubMed]
    [Google Scholar]
  28. Lazdunski A. M., Ventre I., Sturgis J. N.( 2004). Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2:581–592 [View Article][PubMed]
    [Google Scholar]
  29. Lee J. H., Lee J.( 2010). Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34:426–444[PubMed]
    [Google Scholar]
  30. Lee Y., Peña-Llopis S., Kang Y. S., Shin H. D., Demple B., Madsen E. L., Jeon C. O., Park W.( 2006). Expression analysis of the fpr (ferredoxin-NADP+ reductase) gene in Pseudomonas putida KT2440. Biochem Biophys Res Commun 339:1246–1254 [View Article][PubMed]
    [Google Scholar]
  31. Lee J., Jayaraman A., Wood T. K.( 2007). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7:42 [View Article][PubMed]
    [Google Scholar]
  32. Lee J., Attila C., Cirillo S. L., Cirillo J. D., Wood T. K.( 2009). Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2:75–90 [View Article][PubMed]
    [Google Scholar]
  33. Lee H. H., Molla M. N., Cantor C. R., Collins J. J.( 2010a). Bacterial charity work leads to population-wide resistance. Nature 467:82–85 [View Article][PubMed]
    [Google Scholar]
  34. Lee Y., Yeom J., Kim J., Jung J., Jeon C. O., Park W.( 2010b). Phenotypic and physiological alterations by heterologous acylhomoserine lactone synthase expression in Pseudomonas putida. Microbiology 156:3762–3772 [View Article][PubMed]
    [Google Scholar]
  35. Lee J. H., Cho H. S., Kim Y., Kim J. A., Banskota S., Cho M. H., Lee J.( 2013). Indole and 7-benzyloxyindole attenuate the virulence of Staphylococcus aureus. Appl Microbiol Biotechnol 97:4543–4552 [View Article][PubMed]
    [Google Scholar]
  36. Marketon M. M., González J. E.( 2002). Identification of two quorum-sensing systems in Sinorhizobium meliloti. J Bacteriol 184:3466–3475 [View Article][PubMed]
    [Google Scholar]
  37. Miller J. H.( 1992). A Short Course in Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  38. Missiakas D., Schwager F., Betton J. M., Georgopoulos C., Raina S.( 1996). Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli.. EMBO J 15:6899–6909[PubMed]
    [Google Scholar]
  39. Nikaido E., Giraud E., Baucheron S., Yamasaki S., Wiedemann A., Okamoto K., Takagi T., Yamaguchi A., Cloeckaert A., Nishino K.( 2012). Effects of indole on drug resistance and virulence of Salmonella enterica serovar Typhimurium revealed by genome-wide analyses. Gut Pathog 4:5 [View Article][PubMed]
    [Google Scholar]
  40. Niu C., Clemmer K. M., Bonomo R. A., Rather P. N.( 2008). Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. J Bacteriol 190:3386–3392 [View Article][PubMed]
    [Google Scholar]
  41. Piñero-Fernandez S., Chimerel C., Keyser U. F., Summers D. K.( 2011). Indole transport across Escherichia coli membranes. J Bacteriol 193:1793–1798 [View Article][PubMed]
    [Google Scholar]
  42. Rader B. A., Campagna S. R., Semmelhack M. F., Bassler B. L., Guillemin K.( 2007). The quorum-sensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori. J Bacteriol 189:6109–6117 [View Article][PubMed]
    [Google Scholar]
  43. Rosenberg M., Bayer E. A., Delarea J., Rosenberg E.( 1982). Role of thin fimbriae in adherence and growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. Appl Environ Microbiol 44:929–937[PubMed]
    [Google Scholar]
  44. Sabag-Daigle A., Soares J. A., Smith J. N., Elmasry M. E., Ahmer B. M.( 2012). The acyl homoserine lactone receptor, SdiA, of Escherichia coli and Salmonella enterica serovar Typhimurium does not respond to indole. Appl Environ Microbiol 78:5424–5431 [View Article][PubMed]
    [Google Scholar]
  45. Sarkar S., Chakraborty R.( 2008). Quorum sensing in metal tolerance of Acinetobacter junii BB1A is associated with biofilm production. FEMS Microbiol Lett 282:160–165 [View Article][PubMed]
    [Google Scholar]
  46. Sasaki-Imamura T., Yano A., Yoshida Y.( 2010). Production of indole from L-tryptophan and effects of these compounds on biofilm formation by Fusobacterium nucleatum ATCC 25586. Appl Environ Microbiol 76:4260–4268 [View Article][PubMed]
    [Google Scholar]
  47. Seo H., Kim J., Jung J., Jin H. M., Jeon C. O., Park W.( 2012). Complexity of cell-cell interactions between Pseudomonas sp. AS1 and Acinetobacter oleivorans DR1: metabolic commensalism, biofilm formation and quorum quenching. Res Microbiol 163:173–181 [View Article][PubMed]
    [Google Scholar]
  48. Sims J., Renwick A. G.( 1983). The effects of saccharin on the metabolism of dietary tryptophan to indole, a known cocarcinogen for the urinary bladder of the rat. Toxicol Appl Pharmacol 67:132–151 [View Article][PubMed]
    [Google Scholar]
  49. Stanley N. R., Lazazzera B. A.( 2004). Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol 52:917–924 [View Article][PubMed]
    [Google Scholar]
  50. Swem L. R., Swem D. L., O’Loughlin C. T., Gatmaitan R., Zhao B., Ulrich S. M., Bassler B. L.( 2009). A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell 35:143–153 [View Article][PubMed]
    [Google Scholar]
  51. Tomaras A. P., Flagler M. J., Dorsey C. W., Gaddy J. A., Actis L. A.( 2008). Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology 154:3398–3409 [View Article][PubMed]
    [Google Scholar]
  52. Vannini A., Volpari C., Gargioli C., Muraglia E., Cortese R., De Francesco R., Neddermann P., Marco S. D.( 2002). The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21:4393–4401 [View Article][PubMed]
    [Google Scholar]
  53. Vega N. M., Allison K. R., Khalil A. S., Collins J. J.( 2012). Signaling-mediated bacterial persister formation. Nat Chem Biol 8:431–433 [View Article][PubMed]
    [Google Scholar]
  54. Watanabe K., Kodama Y., Harayama S.( 2001). Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting. J Microbiol Methods 44:253–262 [View Article][PubMed]
    [Google Scholar]
  55. Waters C. M., Lu W., Rabinowitz J. D., Bassler B. L.( 2008). Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190:2527–2536 [View Article][PubMed]
    [Google Scholar]
  56. Weiss L. E., Badalamenti J. P., Weaver L. J., Tascone A. R., Weiss P. S., Richard T. L., Cirino P. C.( 2008). Engineering motility as a phenotypic response to LuxI/R-dependent quorum sensing in Escherichia coli. Biotechnol Bioeng 100:1251–1255 [View Article][PubMed]
    [Google Scholar]
  57. Williams P.( 2007). Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938 [View Article][PubMed]
    [Google Scholar]
  58. Yanofsky C.( 2007). RNA-based regulation of genes of tryptophan synthesis and degradation, in bacteria. RNA 13:1141–1154 [View Article][PubMed]
    [Google Scholar]
  59. Zhang R. G., Pappas K. M., Brace J. L., Miller P. C., Oulmassov T., Molyneaux J. M., Anderson J. C., Bashkin J. K., Winans S. C., Joachimiak A.( 2002). Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971–974 [View Article][PubMed]
    [Google Scholar]
  60. Zhu J., Winans S. C.( 2001). The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci U S A 98:1507–1512 [View Article][PubMed]
    [Google Scholar]
  61. Zhu J., Miller M. B., Vance R. E., Dziejman M., Bassler B. L., Mekalanos J. J.( 2002). Quorum-sensing regulators control virulence gene expression in Vibrio cholerae.. Proc Natl Acad Sci U S A 99:3129–3134 [View Article][PubMed]
    [Google Scholar]
  62. Zuccato E., Venturi M., Di Leo G., Colombo L., Bertolo C., Doldi S. B., Mussini E.( 1993). Role of bile acids and metabolic activity of colonic bacteria in increased risk of colon cancer after cholecystectomy. Dig Dis Sci 38:514–519 [View Article][PubMed]
    [Google Scholar]
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