1887

Abstract

The development of biofilm requires the differential expression of various genes implicated in cell signalling, stress responses, motility and the synthesis of structures responsible for cell attachment. The operon is among the stress-response genes most induced during growth of the biofilm. In this study we demonstrated, to our knowledge for the first time, that the lack of IbpAB proteins in cells inhibited the formation of biofilm at the air–liquid interface, although it allowed normal planktonic growth. We showed that mutant cells experienced endogenous oxidative stress, which might result from a decreased catalase activity. The endogenous oxidative stress in cells led to increased expression of tryptophanase, an enzyme which catalyses the synthesis of indole. We demonstrated that the formation of biofilm by the mutant was delayed due to the increase in the extracellular concentration of indole, which is known to play the role of a signal molecule, inhibiting biofilm growth.

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2010-01-01
2019-10-19
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References

  1. Allen, S. P., Polazzi, J. O., Gierse, J. K. & Easton, A. M. ( 1992; ). Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol 174, 6938–6947.
    [Google Scholar]
  2. Beloin, C., Valle, J., Latour-Lambert, P., Faure, P., Kzreminski, M., Balestrino, D., Haagensen, J. A., Molin, S., Prensier, G. & other authors ( 2004; ). Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51, 659–674.
    [Google Scholar]
  3. Blankenhorn, D., Phillips, J. & Slonczewski, J. L. ( 1999; ). Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J Bacteriol 181, 2209–2216.
    [Google Scholar]
  4. Choi, S. S., Kang, B. Y., Chung, M. J., Kim, S. D., Park, S. H., Kim, J. S., Kang, C. Y. & Ha, N. J. ( 2005; ). Safety assessment of potential lactic acid bacteria Bifidobacterium longum SPM1205 isolated from healthy Koreans. J Microbiol 43, 493–498.
    [Google Scholar]
  5. Chuang, S. E., Burland, V., Plunkett, G., III, Daniels, D. L. & Blattner, F. R. ( 1993; ). Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene 134, 1–6.[CrossRef]
    [Google Scholar]
  6. Churchward, G., Belin, D. & Nagamine, Y. ( 1984; ). A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene 31, 165–171.[CrossRef]
    [Google Scholar]
  7. Collet, A., Vilain, S., Cosette, P., Junter, G. A., Jouenne, T., Phillips, R. S. & Di Martino, P. ( 2007; ). Protein expression in Escherichia coli S17-1 biofilms: impact of indole. Antonie Van Leeuwenhoek 91, 71–85.
    [Google Scholar]
  8. Colón-González, M., Méndez-Ortiz, M. M. & Membrillo-Hernández, J. ( 2004; ). Anaerobic growth does not support biofilm formation in Escherichia coli K-12. Res Microbiol 155, 514–521.[CrossRef]
    [Google Scholar]
  9. Di Martino, P., Fursy, R., Bret, L., Sundararaju, B. & Phillips, R. S. ( 2003; ). Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can J Microbiol 49, 443–449.[CrossRef]
    [Google Scholar]
  10. Domka, J., Lee, J. & Wood, T. K. ( 2006; ). YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol 72, 2449–2459.[CrossRef]
    [Google Scholar]
  11. Domka, J., Lee, J., Bansal, T. & Wood, T. K. ( 2007; ). Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol 9, 332–346.[CrossRef]
    [Google Scholar]
  12. Dubern, J. F., Lagendijk, E. L., Lugtenberg, B. J. & Bloemberg, G. V. ( 2005; ). The heat shock genes dnaK, dnaJ, and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J Bacteriol 187, 5967–5976.[CrossRef]
    [Google Scholar]
  13. Echave, P., Tamarit, J., Cabiscol, E. & Ros, J. ( 2003; ). Novel antioxidant role of alcohol dehydrogenase E from Escherichia coli. J Biol Chem 278, 30193–30198.[CrossRef]
    [Google Scholar]
  14. Fux, C. A., Costerton, J. W., Stewart, P. S. & Stoodley, P. ( 2005; ). Survival strategies of infectious biofilms. Trends Microbiol 13, 34–40.[CrossRef]
    [Google Scholar]
  15. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. ( 2004; ). Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95–108.[CrossRef]
    [Google Scholar]
  16. Harrison, J. J., Ceri, H. & Turner, R. J. ( 2007; ). Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5, 928–938.[CrossRef]
    [Google Scholar]
  17. Haslbeck, M., Franzmann, T., Weinfurtner, D. & Buchner, J. ( 2005; ). Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12, 842–846.[CrossRef]
    [Google Scholar]
  18. Jakubowski, W., Biliński, T. & Bartosz, G. ( 2000; ). Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. Free Radic Biol Med 28, 659–664.[CrossRef]
    [Google Scholar]
  19. Junker, L. M., Toba, F. A. & Hay, A. G. ( 2007; ). Transcription in Escherichia coli PHL628 biofilms. FEMS Microbiol Lett 268, 237–243.[CrossRef]
    [Google Scholar]
  20. Kershaw, C. J., Brown, N. L., Constantinidou, C., Patel, M. D. & Hobman, J. L. ( 2005; ). The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151, 1187–1198.[CrossRef]
    [Google Scholar]
  21. Kitagawa, M., Miyakawa, M., Matsumura, Y. & Tsuchido, T. ( 2000; ). Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stress in Escherichia coli. FEMS Microbiol Lett 184, 165–171.[CrossRef]
    [Google Scholar]
  22. Kitagawa, M., Miyakawa, M., Matsumura, Y. & Tsuchido, T. ( 2002; ). Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269, 2907–2917.[CrossRef]
    [Google Scholar]
  23. Kuczyńska-Wisńik, D., Laskowska, E. & Taylor, A. ( 2001; ). Transcription of the ibpB heat-shock gene is under control of σ 32- and σ 54-promoters, a third regulon of heat-shock response. Biochem Biophys Res Commun 284, 57–64.[CrossRef]
    [Google Scholar]
  24. Kuczyńska-Wisńik, D., Kędzierska, S., Matuszewska, E., Lund, P., Taylor, A., Lipińska, B. & Laskowska, E. ( 2002; ). The Escherichia coli small heat-shock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock. Microbiology 148, 1757–1765.
    [Google Scholar]
  25. Lacour, S. & Landini, P. ( 2004; ). σ S-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σ S-dependent genes and identification of their promoter sequences. J Bacteriol 186, 7186–7195.[CrossRef]
    [Google Scholar]
  26. Laskowska, E., Wawrzynów, A. & Taylor, A. ( 1996; ). IbpA and IbpB, the new heat shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78, 117–122.[CrossRef]
    [Google Scholar]
  27. Laskowska, E., Kuczyńska-Wiśnik, D., Bąk, M. & Lipińska, B. ( 2003; ). Trimethoprim induces heat shock proteins and protein aggregation in E. coli cells. Curr Microbiol 47, 286–289.[CrossRef]
    [Google Scholar]
  28. Lee, J., Jayaraman, A. & Wood, T. K. ( 2007; ). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7, 42 [CrossRef]
    [Google Scholar]
  29. Lee, J., Zhang, X. S., Hegde, M., Bentley, W. E., Jayaraman, A. & Wood, T. K. ( 2008; ). Indole cell signaling occurs primarily at low temperatures in Escherichia coli. ISME J 2, 1007–1023.[CrossRef]
    [Google Scholar]
  30. Matuszewska, M., Kuczyńska-Wiśnik, D., Laskowska, E. & Liberek, K. ( 2005; ). The small heat shock protein IbpA from Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem 280, 12292–12298.[CrossRef]
    [Google Scholar]
  31. Matuszewska, E., Kwiatkowska, J., Kuczyńska-Wiśnik, D. & Laskowska, E. ( 2008; ). Escherichia coli heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper. Microbiology 154, 1739–1747.[CrossRef]
    [Google Scholar]
  32. Mogk, A., Deuerling, E., Vorderwülbecke, S., Vierling, E. & Bukau, B. ( 2003a; ). Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50, 585–595.[CrossRef]
    [Google Scholar]
  33. Mogk, A., Schlieker, C., Friedrich, K. L., Schönfeld, H. J., Vierling, E. & Bukau, B. ( 2003b; ). Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278, 31033–31042.[CrossRef]
    [Google Scholar]
  34. Nakamoto, H. & Vigh, L. ( 2007; ). The small heat shock proteins and their clients. Cell Mol Life Sci 64, 294–306.[CrossRef]
    [Google Scholar]
  35. Nobre, L. S., Al-Shahrour, F., Dopazo, J. & Saraiva, L. M. ( 2009; ). Exploring the antimicrobial action of a carbon monoxide-releasing compound through whole-genome transcription profiling of Escherichia coli. Microbiology 155, 813–824.[CrossRef]
    [Google Scholar]
  36. Peréz, J. M., Calderón, I. L., Arenas, F. A., Fuentes, D. E., Pradenas, G. A., Fuentes, E. L., Sandoval, J. M., Castro, M. E., Elías, A. O. & Vásquez, C. C. ( 2007; ). Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS One 2, e211 [CrossRef]
    [Google Scholar]
  37. Pomposiello, P. J., Bennik, M. H. & Demple, B. ( 2001; ). Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183, 3890–3902.[CrossRef]
    [Google Scholar]
  38. Prüß, B. M., Besemann, C., Denton, A. & Wolfe, A. J. ( 2006; ). A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol 188, 3731–3739.[CrossRef]
    [Google Scholar]
  39. Ratajczak, E., Zietkiewicz, S. & Liberek, K. ( 2009; ). Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J Mol Biol 386, 178–189.[CrossRef]
    [Google Scholar]
  40. Ren, D., Bedzyk, L. A., Thomas, S. M., Ye, R. W. & Wood, T. K. ( 2004; ). Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64, 515–524.[CrossRef]
    [Google Scholar]
  41. Sambrook, J., Fritsh, E. F. & Maniatis, F. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn.Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Schembri, M. A., Kjaergaard, K. & Klemm, P. ( 2003; ). Global gene expression in Escherichia coli biofilms. Mol Microbiol 48, 253–267.[CrossRef]
    [Google Scholar]
  43. Shi, W., Zhou, Y., Wild, J., Adler, J. & Gross, C. A. ( 1992; ). DnaK, DnaJ, and GrpE are required for flagellum synthesis in Escherichia coli. J Bacteriol 174, 6256–6263.
    [Google Scholar]
  44. Shigapova, N., Török, Z., Balogh, G., Goloubinoff, P., Vígh, L. & Horváth, I. ( 2005; ). Membrane fluidization triggers membrane remodeling which affects the thermotolerance in Escherichia coli. Biochem Biophys Res Commun 328, 1216–1223.[CrossRef]
    [Google Scholar]
  45. Stewart, P. S. & Franklin, M. J. ( 2008; ). Physiological heterogeneity in biofilms. Nat Rev Microbiol 6, 199–210.[CrossRef]
    [Google Scholar]
  46. Suwalsky, M., Ungerer, B., Quevedo, L., Aguilar, F. & Sotomayor, C. P. ( 1998; ). Cu2+ ions interact with cell membranes. J Inorg Biochem 70, 233–238.[CrossRef]
    [Google Scholar]
  47. Tamarit, J., Cabiscol, E. & Ros, J. ( 1998; ). Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273, 3027–3032.[CrossRef]
    [Google Scholar]
  48. Van Houdt, R. & Michiels, C. W. ( 2005; ). Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res Microbiol 156, 626–633.[CrossRef]
    [Google Scholar]
  49. Veinger, L., Diamant, S., Buchner, J. & Goloubinoff, P. ( 1998; ). The small heat-shock protein IbpB from Escherichia coli stabilizes stress denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273, 11032–11037.[CrossRef]
    [Google Scholar]
  50. Visick, J. E. & Clarke, S. ( 1997; ). RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol 179, 4158–4163.
    [Google Scholar]
  51. Wang, D., Ding, X. & Rather, P. N. ( 2001; ). Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183, 4210–4216.[CrossRef]
    [Google Scholar]
  52. Wood, T. K. ( 2009; ). Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11, 1–15.[CrossRef]
    [Google Scholar]
  53. Zhang, X. S., García-Contreras, R. & Wood, T. K. ( 2007; ). YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol 189, 3051–3062.[CrossRef]
    [Google Scholar]
  54. Zheng, M., Wang, X., Templeton, L. J., Smulski, D. R., La Rossa, R. A. & Storz, G. ( 2001; ). DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183, 4562–4570.[CrossRef]
    [Google Scholar]
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