1887

Abstract

Transposition activity in bacteria is generally maintained at a low level. The activity of mobile DNA elements can be controlled by bacterially encoded global regulators. Regulation of transposition of Tn in is one such example. Activation of transposition of Tn in starving bacteria requires the stationary-phase sigma factor RpoS and integration host factor (IHF). IHF plays a dual role in Tn translocation by activating transcription of the transposase gene of the transposon and facilitating TnpA binding to the inverted repeats of the transposon. Our previous results have indicated that besides IHF some other -encoded global regulator(s) might bind to the ends of Tn and regulate transposition activity. In this study, employing a DNase I footprint assay we have identified a binding site of Fis (factor for inversion stimulation) centred 135 bp inside the left end of Tn. Our results of gel mobility shift and DNase I footprint studies revealed that Fis out-competes IHF from the left end of Tn, thereby abolishing the binding of TnpA. Thus, the results obtained in this study indicate that the transposition of Tn is regulated by the cellular amount of global regulators Fis and IHF.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022830-0
2009-04-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/4/1203.html?itemId=/content/journal/micro/10.1099/mic.0.022830-0&mimeType=html&fmt=ahah

References

  1. Adams, M. H. ( 1959; ). Bacteriophages. New York: Interscience Publishers.
  2. Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S. & Ishihama, A. ( 1999; ). Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181, 6361–6370.
    [Google Scholar]
  3. Amzallag, G. N. ( 2004; ). Adaptive changes in bacteria: a consequence of nonlinear transitions in chromosome topology? J Theor Biol 229, 361–369.[CrossRef]
    [Google Scholar]
  4. Azam, T. A. & Ishihama, A. ( 1999; ). Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274, 33105–33113.[CrossRef]
    [Google Scholar]
  5. Bayley, S. A., Duggleby, C. J., Worsey, M. J., Williams, P. A., Hardy, K. G. & Broda, P. ( 1977; ). Two modes of loss of the Tol function from Pseudomonas putida mt-2. Mol Gen Genet 154, 203–204.[CrossRef]
    [Google Scholar]
  6. Beach, M. B. & Osuna, R. ( 1998; ). Identification and characterization of the fis operon in enteric bacteria. J Bacteriol 180, 5932–5946.
    [Google Scholar]
  7. Bertani, I., Sevo, M., Kojic, M. & Venturi, V. ( 2003; ). Role of GacA, LasI, RhlI, Ppk, PsrA, Vfr and ClpXP in the regulation of the stationary-phase sigma factor rpoS/RpoS in Pseudomonas. Arch Microbiol 180, 264–271.[CrossRef]
    [Google Scholar]
  8. Betermier, M., Lefrere, V., Koch, C., Alazard, R. & Chandler, M. ( 1989; ). The Escherichia coli protein, Fis: specific binding to the ends of phage Mu DNA and modulation of phage growth. Mol Microbiol 3, 459–468.[CrossRef]
    [Google Scholar]
  9. Betermier, M., Poquet, I., Alazard, R. & Chandler, M. ( 1993; ). Involvement of Escherichia coli FIS protein in maintenance of bacteriophage mu lysogeny by the repressor: control of early transcription and inhibition of transposition. J Bacteriol 175, 3798–3811.
    [Google Scholar]
  10. Betermier, M., Galas, D. J. & Chandler, M. ( 1994; ). Interaction of Fis protein with DNA: bending and specificity of binding. Biochimie 76, 958–967.[CrossRef]
    [Google Scholar]
  11. Boswell, S., Mathew, J., Beach, M., Osuna, R. & Colon, W. ( 2004; ). Variable contributions of tyrosine residues to the structural and spectroscopic properties of the factor for inversion stimulation. Biochemistry 43, 2964–2977.[CrossRef]
    [Google Scholar]
  12. Bradley, M. D., Beach, M. B., de Koning, A. P., Pratt, T. S. & Osuna, R. ( 2007; ). Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology 153, 2922–2940.[CrossRef]
    [Google Scholar]
  13. Chandler, M. & Mahillon, J. ( 2002; ). Insertion sequences revisted. In Mobile DNA II, pp. 305–366. Edited by N. L. Craig, R. Craigie, M. Gellert & A. M. Lambowitz. Washington, DC: American Society for Microbiology.
  14. Dorgai, L., Oberto, J. & Weisberg, R. A. ( 1993; ). Xis and Fis proteins prevent site-specific DNA inversion in lysogens of phage HK022. J Bacteriol 175, 693–700.
    [Google Scholar]
  15. Doolittle, W. F., Kirkwood, T. B. & Dempster, M. A. ( 1984; ). Selfish DNAs with self-restraint. Nature 307, 501–502.
    [Google Scholar]
  16. Finkel, S. E. & Johnson, R. C. ( 1992; ). The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol 6, 3257–3265.[CrossRef]
    [Google Scholar]
  17. Gonzalez-Gil, G., Bringmann, P. & Kahmann, R. ( 1996; ). FIS is a regulator of metabolism in Escherichia coli. Mol Microbiol 22, 21–29.[CrossRef]
    [Google Scholar]
  18. Goosen, N. & van de Putte, P. ( 1995; ). The regulation of transcription initiation by integration host factor. Mol Microbiol 16, 1–7.[CrossRef]
    [Google Scholar]
  19. Gutierrez-Rios, R. M., Freyre-Gonzalez, J. A., Resendis, O., Collado-Vides, J., Saier, M. & Gosset, G. ( 2007; ). Identification of regulatory network topological units coordinating the genome-wide transcriptional response to glucose in Escherichia coli. BMC Microbiol 7, 53 [CrossRef]
    [Google Scholar]
  20. Hengen, P. N., Bartram, S. L., Stewart, L. E. & Schneider, T. D. ( 1997; ). Information analysis of Fis binding sites. Nucleic Acids Res 25, 4994–5002.[CrossRef]
    [Google Scholar]
  21. Hõrak, R. & Kivisaar, M. ( 1998; ). Expression of the transposase gene tnpA of Tn4652 is positively affected by integration host factor. J Bacteriol 180, 2822–2829.
    [Google Scholar]
  22. Hõrak, R. & Kivisaar, M. ( 1999; ). Regulation of the transposase of Tn4652 by the transposon-encoded protein TnpC. J Bacteriol 181, 6312–6318.
    [Google Scholar]
  23. Ilves, H., Hõrak, R. & Kivisaar, M. ( 2001; ). Involvement of σ S in starvation-induced transposition of Pseudomonas putida transposon Tn4652. J Bacteriol 183, 5445–5448.[CrossRef]
    [Google Scholar]
  24. Ilves, H., Hõrak, R., Teras, R. & Kivisaar, M. ( 2004; ). IHF is the limiting host factor in transposition of Pseudomonas putida transposon Tn4652 in stationary phase. Mol Microbiol 51, 1773–1785.[CrossRef]
    [Google Scholar]
  25. Johnson, R. C., Bruist, M. F. & Simon, M. I. ( 1986; ). Host protein requirements for in vitro site-specific DNA inversion. Cell 46, 531–539.[CrossRef]
    [Google Scholar]
  26. Kasak, L., Hõrak, R. & Kivisaar, M. ( 1997; ). Promoter-creating mutations in Pseudomonas putida: a model system for the study of mutation in starving bacteria. Proc Natl Acad Sci U S A 94, 3134–3139.[CrossRef]
    [Google Scholar]
  27. Kugelberg, E., Lofmark, S., Wretlind, B. & Andersson, D. I. ( 2005; ). Reduction of the fitness burden of quinolone resistance in Pseudomonas aeruginosa. J Antimicrob Chemother 55, 22–30.
    [Google Scholar]
  28. Lei, G. S., Chen, C. J., Yuan, H. S., Wang, S. H. & Hu, S. T. ( 2007; ). Inhibition of IS2 transposition by factor for inversion stimulation. FEMS Microbiol Lett 275, 98–105.[CrossRef]
    [Google Scholar]
  29. Martinez-Antonio, A. & Collado-Vides, J. ( 2003; ). Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6, 482–489.[CrossRef]
    [Google Scholar]
  30. Miller, J. H. ( 1992; ). A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  31. Pan, C. Q., Finkel, S. E., Cramton, S. E., Feng, J. A., Sigman, D. S. & Johnson, R. C. ( 1996; ). Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. J Mol Biol 264, 675–695.[CrossRef]
    [Google Scholar]
  32. Salgado, H., Gama-Castro, S., Martinez-Antonio, A., Díaz-Peredo, E., Sánchez-Solano, F., Peralta-Gil, M., Garcia-Alonso, D., Jiménez-Jacinto, V., Santos-Zavaleta, A. & other authors ( 2004; ). RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12. Nucleic Acids Res 32, D303–D306.[CrossRef]
    [Google Scholar]
  33. Schneider, R., Travers, A., Kutateladze, T. & Muskhelishvili, G. ( 1999; ). A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol 34, 953–964.[CrossRef]
    [Google Scholar]
  34. Schneider, R., Lurz, R., Luder, G., Tolksdorf, C., Travers, A. & Muskhelishvili, G. ( 2001; ). An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res 29, 5107–5114.[CrossRef]
    [Google Scholar]
  35. Shao, Y., Feldman-Cohen, L. S. & Osuna, R. ( 2008; ). Functional characterization of the Escherichia coli Fis-DNA binding sequence. J Mol Biol 376, 771–785.[CrossRef]
    [Google Scholar]
  36. Sharma, R. C. & Schimke, R. T. ( 1996; ). Preparation of electrocompetent E. coli using salt-free growth medium. Biotechniques 20, 42–44.
    [Google Scholar]
  37. Skoko, D., Yoo, D., Bai, H., Schnurr, B., Yan, J., McLeod, S. M., Marko, J. F. & Johnson, R. C. ( 2006; ). Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J Mol Biol 364, 777–798.[CrossRef]
    [Google Scholar]
  38. Spurio, R., Falconi, M., Brandi, A., Pon, C. L. & Gualerzi, C. O. ( 1997; ). The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J 16, 1795–1805.[CrossRef]
    [Google Scholar]
  39. Studier, F. W. & Moffatt, B. A. ( 1986; ). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113–130.[CrossRef]
    [Google Scholar]
  40. Swinger, K. K., Lemberg, K. M., Zhang, Y. & Rice, P. A. ( 2003; ). Flexible DNA bending in HU-DNA cocrystal structures. EMBO J 22, 3749–3760.[CrossRef]
    [Google Scholar]
  41. Teras, R., Hõrak, R. & Kivisaar, M. ( 2000; ). Transcription from fusion promoters generated during transposition of transposon Tn4652 is positively affected by integration host factor in Pseudomonas putida. J Bacteriol 182, 589–598.[CrossRef]
    [Google Scholar]
  42. Travers, A. & Muskhelishvili, G. ( 2005a; ). DNA supercoiling – a global transcriptional regulator for enterobacterial growth? Nat Rev Microbiol 3, 157–169.[CrossRef]
    [Google Scholar]
  43. Travers, A. & Muskhelishvili, G. ( 2005b; ). Bacterial chromatin. Curr Opin Genet Dev 15, 507–514.[CrossRef]
    [Google Scholar]
  44. Travers, A., Schneider, R. & Muskhelishvili, G. ( 2001; ). DNA supercoiling and transcription in Escherichia coli: the FIS connection. Biochimie 83, 213–217.[CrossRef]
    [Google Scholar]
  45. Tsuda, M. & Iino, T. ( 1987; ). Genetic analysis of a transposon carrying toluene degrading genes on a TOL plasmid pWW0. Mol Gen Genet 210, 270–276.[CrossRef]
    [Google Scholar]
  46. Valls, M., Buckle, M. & de Lorenzo, V. ( 2002; ). In vivo UV laser footprinting of the Pseudomonas putida sigma 54Pu promoter reveals that integration host factor couples transcriptional activity to growth phase. J Biol Chem 277, 2169–2175.[CrossRef]
    [Google Scholar]
  47. Ward, C. M., Wardle, S. J., Singh, R. K. & Haniford, D. B. ( 2007; ). The global regulator H-NS binds to two distinct classes of sites within the Tn10 transpososome to promote transposition. Mol Microbiol 64, 1000–1013.[CrossRef]
    [Google Scholar]
  48. Wardle, S. J., O'Carroll, M., Derbyshire, K. M. & Haniford, D. B. ( 2005; ). The global regulator H-NS acts directly on the transpososome to promote Tn10 transposition. Genes Dev 19, 2224–2235.[CrossRef]
    [Google Scholar]
  49. Weinreich, M. D. & Reznikoff, W. S. ( 1992; ). Fis plays a role in Tn5 and IS50 transposition. J Bacteriol 174, 4530–4537.
    [Google Scholar]
  50. Wiater, L. A. & Grindley, N. D. ( 1988; ). Gamma delta transposase and integration host factor bind cooperatively at both ends of gamma delta. EMBO J 7, 1907–1911.
    [Google Scholar]
  51. Xu, J. & Johnson, R. C. ( 1995; ). Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol 177, 938–947.
    [Google Scholar]
  52. Yuste, L., Hervas, A. B., Canosa, I., Tobes, R., Jiménez, J. I., Nogales, J., Pérez-Pérez, M. M., Santero, E., Díaz, E. & other authors ( 2006; ). Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ Microbiol 8, 165–177.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022830-0
Loading
/content/journal/micro/10.1099/mic.0.022830-0
Loading

Data & Media loading...

Supplements

Oligonucleotides used in this study [ PDF] (11 kb) PCR-amplified DNA fragments used in gel mobility shift and DNase I footprint assays [ PDF] (11 kb)

PDF

Oligonucleotides used in this study [ PDF] (11 kb) PCR-amplified DNA fragments used in gel mobility shift and DNase I footprint assays [ PDF] (11 kb)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error