Indole inhibits bacterial quorum sensing signal transmission by interfering with quorum sensing regulator folding

Microbiology (United Kingdom)

Volumn 159, Issue PART 12, 2013, Pages 2616-2625

  Kim, Jisun ^a   Park, Woojun ^a  

^a Korea University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINASE; CHAPERONE; INDOLE; MESSENGER RNA; METHIONINE; N ACYLHOMOSERINE LACTONE; PROTEINASE;

ACINETOBACTER; ARTICLE; BIODEGRADATION; BIOFILM; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; GENE INDUCTION; LIQUID CULTURE; NONHUMAN; NORTHERN BLOTTING; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN STABILITY; PSEUDOMONAS PUTIDA; QUORUM SENSING; RHIZOBIUM RADIOBACTER; SIGNAL TRANSDUCTION; TURNOVER TIME;

ACINETOBACTER; ACYL-BUTYROLACTONES; AGROBACTERIUM TUMEFACIENS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; INDOLES; PROTEIN BINDING; PROTEIN FOLDING; QUORUM SENSING; TRANSCRIPTION FACTORS;

EID: 84888859299     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.070615-0     Document Type: Article

References (62)

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.
2. Botsford, J. L. & Demoss, R. D. (1972). Escherichia coli tryptophanase in the enteric environment. J Bacteriol 109, 74-80.
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.
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.
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.
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.
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.
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.
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.
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.
11. Gaddy, J. A. & Actis, L. A. (2009). Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol 4, 273-278.
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.
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.
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 ArgentMicrobiol 41, 73-78.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
28. Lazdunski, A. M., Ventre, I. & Sturgis, J. N. (2004). Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2, 581-592.
29. Lee, J. H. & Lee, J. (2010). Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34, 426-444.
30. +reductase) gene in Pseudomonas putida KT2440. Biochem Biophys Res Commun 339, 1246-1254.
31. Lee, J., Jayaraman, A. & Wood, T. K. (2007). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7, 42.
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.
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.
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.
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.
36. Marketon, M. M. & González, J. E. (2002). Identification of two quorum-sensing systems in Sinorhizobium meliloti. J Bacteriol 184, 3466-3475.
37. Miller, J. H. (1992). A Short Course in Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
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.
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.
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.
41. Piñero-Fernandez, S., Chimerel, C., Keyser, U. F. & Summers, D. K. (2011). Indole transport across Escherichia coli membranes. J Bacteriol 193, 1793-1798.
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.
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.
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.
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.
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.
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.
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.
49. Stanley, N. R. & Lazazzera, B. A. (2004). Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol 52, 917-924.
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.
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.
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.
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.
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.
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.
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.
57. Williams, P. (2007). Quorum sensing, communication and crosskingdom signalling in the bacterial world. Microbiology 153, 3923-3938.
58. Yanofsky, C. (2007). RNA-based regulation of genes of tryptophan synthesis and degradation, in bacteria. RNA 13, 1141-1154.
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.
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.
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.
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.