1887

Microbiology

Volume 150, Issue 1

recognizes the promoter of and responds to heat shock in chlamydiae Free

Abstract

The gene of encodes the alternative factor , which bears strong homology to many bacterial factors, including and s and . Recently, a promoter was identified upstream of the late-cycle-expressed gene , which encodes the -histone-like protein 2 ( Yu & Tan, 2003 ). In this study it is shown that the product of chlamydial is an homologue. It was found that recombinant chlamydial , in combination with core RNA polymerase, initiates transcription from the -dependent promoter of . It was also demonstrated that the recombinant chlamydial does not recognize major factor -consensus-like sequences . In -infected cells, two transcripts were detected with 5′ ends located 18 (transcript I) and 54 bp (transcript II) upstream of the translational initiation codon at 16 and 30 h post-infection. When the temperature of cultures infected with was shifted from 35 to 42 °C, the transcript I increased dramatically. The levels of chlamydial , relative to EF-Tu, were greater throughout the exponential growth phase of the reticulate body, but lower late in the developmental cycle. These data support the hypothesis that plays a role in the regulatory network that allows chlamydiae to survive changes in its environment, enabling it to complete its unique developmental cycle.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): EB, elementary body , p.i., post-infection , RB, reticulate body and RNAP, RNA polymerase
© SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26734-0
2004-01-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/1/mic1500205.html?itemId=/content/journal/micro/10.1099/mic.0.26734-0&mimeType=html&fmt=ahah

References

  1. Allen, I., Hatch, T. P. & Pearce, J. H. ( 1985; ). Influence of cysteine deprivation on chlamydial differentiation from reproductive to infective life cycle forms. J Gen Microbiol 131, 3171–3177.
     [Google Scholar]
  2. Beatty, W. L., Byrne, G. I. & Morrison, R. P. ( 1993; ). Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc Natl Acad Sci U S A 90, 3998–4002.[CrossRef]
    [Google Scholar]
  3. Beatty, W. L., Morrison, R. P. & Byrne, G. I. ( 1994; ). Persistent chlamydiae, from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58, 686–699.
     [Google Scholar]
  4. Belland, R. J., Zhong, G., Crane, D. D., Hogan, D., Sturdevant, D., Sharma, J., Beatty, W. L. & Caldwell, H. D. ( 2003; ). Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc Natl Acad Sci U S A 100, 8478–8483.[CrossRef]
    [Google Scholar]
  5. Blattner, F. R., Plunkett, G. I., Bloch, C. A. & 14 other authors ( 1997; ). The complete genome sequence of Escherichia coli K12. Science 277, 1453–1474.[CrossRef]
    [Google Scholar]
  6. Burgess, R. R. & Anthony, L. ( 2001; ). How sigma docks to RNA polymerase and what sigma does. Curr Opin Microbiol 4, 126–131.[CrossRef]
    [Google Scholar]
  7. Caldas, T. D., El Yaagoubi, A. & Richarme, G. ( 1998; ). Chaperone properties of bacterial elongation factor EF-Tu. J Biol Chem 273, 11478–11482.[CrossRef]
    [Google Scholar]
  8. Caldwell, D. H., Kromhout, J. & Schachter, J. ( 1981; ). Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 31, 1161–1176.
     [Google Scholar]
  9. Chang, A. C. & Cohen, S. N. ( 1978; ). Construction and characterization of amplicable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134, 1141–1156.
     [Google Scholar]
  10. Douglas, A. L. & Hatch, T. P. ( 1995; ). Functional analysis of the major outer membrane protein gene promoters of Chlamydia trachomatis. J Bacteriol 177, 6286–6289.
     [Google Scholar]
  11. Douglas, A. L. & Hatch, T. P. ( 2000; ). Expression of the transcripts of the sigma factors and putative sigma factor regulators of Chlamydia trachomatis L2. Gene 247, 209–214.[CrossRef]
    [Google Scholar]
  12. Douglas, A. L., Saxena, N. K. & Hatch, T. P. ( 1994; ). Enhancement of in vitro transcription by addition of cloned, overexpressed major sigma factor of Chlamydia psittaci 6BC. J Bacteriol 176, 4196.
     [Google Scholar]
  13. Dufour, A., Voelker, U., Voelker, A. & Haldenwang, W. G. ( 1996; ). Relative levels and fractionation properties of Bacillus subtilis sigma(B) and its regulators during balanced growth and stress. J Bacteriol 178, 3701–3709.
     [Google Scholar]
  14. Engel, J. N., Pollack, J., Perara, E. & Ganem, D. ( 1990; ). Heat shock response of murine Chlamydia trachomatis. J Bacteriol 172, 6959–6972.
     [Google Scholar]
  15. Fraser, G. M. & Hughes, C. ( 1999; ). Swarming motility. Curr Opin Microbiol 2, 630–635.[CrossRef]
    [Google Scholar]
  16. Grant, S. G. N., Jessee, J., Bloom, F. R. & Hanahan, D. ( 1990; ). Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87, 4645–4649.[CrossRef]
    [Google Scholar]
  17. Gross, C. A., Chan, C., Dombroski, A., Gruber, T., Sharp, M., Tupy, J. & Young, B. ( 1998; ). The functional and regulatory roles of sigma factors in transcription. Cold Spring Harbor Symp Quant Biol 63, 141–155.[CrossRef]
    [Google Scholar]
  18. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. ( 1995; ). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177, 4121–4130.
     [Google Scholar]
  19. Harper, A., Pogson, C. I., Jones, M. L. & Pearce, J. H. ( 2000; ). Chlamydial development is adversely affected by minor changes in amino acid supply, blood plasma amino acid levels, and glucose deprivation. Infect Immun 68, 1457–1464.[CrossRef]
    [Google Scholar]
  20. Hatch, T. P. ( 1999; ). Developmental biology. In Chlamydia. Intracellular Biology, Pathogenesis, and Immunity, pp. 29–67. Edited by R. S. Stephens. Washington, DC: American Society for Microbiology.
  21. Helmann, J. D., Wu, M. F., Kobel, P. A., Gamo, F. J., Wilson, M., Morshedi, M. M., Navre, M. & Paddon, C. ( 2001; ). Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol 183, 7318–7328.[CrossRef]
    [Google Scholar]
  22. Hengge-Aronis, R. ( 1999; ). Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr Opin Microbiol 2, 148–152.[CrossRef]
    [Google Scholar]
  23. Hughes, K. T. & Mathee, K. ( 1998; ). The anti-sigma factors. Annu Rev Microbiol 52, 231–286.[CrossRef]
    [Google Scholar]
  24. Ikebse, T., Iyoda, S. & Kutsukake, K. ( 1999; ). Structure and expression of the fliA operon of Salmonella typhimurium. Microbiology 145, 1389–1396.[CrossRef]
    [Google Scholar]
  25. Ishihama, A. ( 2000; ). Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54, 499–518.[CrossRef]
    [Google Scholar]
  26. Kalman, S., Mitchell, W., Marathe, R. & 7 other authors ( 1999; ). Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat Genet 21, 385–389.[CrossRef]
    [Google Scholar]
  27. Komeda, Y., Kutsukake, K. & Iino, T. ( 1980; ). Definition of additional flagellar genes in Escherichia coli K12. Genetics 94, 277–290.
     [Google Scholar]
  28. Kramer, M. J. & Gordon, F. B. ( 1971; ). Ultrastructural analysis of the effects of penicillin and chlortetracycline on the development of a genital tract Chlamydia. Infect Immun 3, 333–341.
     [Google Scholar]
  29. Kundu, T. K., Kusano, S. & Ishihama, A. ( 1997; ). Promoter selectivity of Escherichia coli RNA polymerase sigmaF holoenzyme involved in transcription of flagellar and chemotaxis genes. J Bacteriol 179, 4264–4269.
     [Google Scholar]
  30. Liu, X. & Matsumura, P. ( 1995; ). An alternative sigma factor controls transcription of flagellar class-III operons in Escherichia coli: gene sequence, overproduction, purification and characterization. Gene 164, 81–84.[CrossRef]
    [Google Scholar]
  31. Liu, X. & Matsumura, P. ( 1996; ). Differential regulation of multiple overlapping promoters in flagellar class II operons in Escherichia coli. Mol Microbiol 21, 613–620.[CrossRef]
    [Google Scholar]
  32. Lonetto, M., Gribskov, M. & Gross, C. A. ( 1992; ). The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174, 3843–3849.
     [Google Scholar]
  33. Macnab, R. M. ( 1996; ). Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 123–145. Edited by F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
  34. Mathews, S. A. & Stephens, R. S. ( 1999; ). DNA structure and novel amino and carboxyl termini of the Chlamydia sigma 70 analogue modulate promoter recognition. Microbiology 145, 1671–1681.[CrossRef]
    [Google Scholar]
  35. Mathews, S. A., Douglas, A., Sriprakash, K. S. & Hatch, T. P. ( 1993; ). In vitro transcription in Chlamydia psittaci and Chlamydia trachomatis. Mol Microbiol 7, 937–946.[CrossRef]
    [Google Scholar]
  36. Mathews, S. A., Volp, K. M. & Timms, P. ( 1999; ). Development of a quantitative gene expression assay for Chlamydia trachomatis identified temporal expression of σ factors. FEBS Lett 458, 354–358.[CrossRef]
    [Google Scholar]
  37. Matsumoto, A. & Manire, G. P. ( 1970; ). Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J Bacteriol 101, 278–285.
     [Google Scholar]
  38. Miller, D. L. & Weissbach, H. ( 1974; ). Elongation factor Tu and the aminoacyl-tRNA-EFTu-GTP complex. Methods Enzymol 30, 219–232.
     [Google Scholar]
  39. Moulder, J. W. ( 1991; ). Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55, 143–190.
     [Google Scholar]
  40. Nicholson, T. L., Olinger, L., Chong, K., Schoolnik, G. & Stephens, R. S. ( 2003; ). Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J Bacteriol 185, 3179–3189.[CrossRef]
    [Google Scholar]
  41. Nicole, E. B. & Dombroski, A. J. ( 2001; ). Isolation and characterization of mutations in region 1.2 of Escherichia coli σ 70. Mol Microbiol 42, 427–437.[CrossRef]
    [Google Scholar]
  42. Raulston, J. E. ( 1997; ). Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect Immun 65, 4539–4547.
     [Google Scholar]
  43. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Laboratory.
  44. Schachter, J. ( 1999; ). Infection and diseases epidemiology. In Chlamydia: Intracellular Biology, Pathogenesis and Immunity, pp. 139–169. Edited by R. S. Stephens. Washington, DC: American Society for Microbiology.
  45. Shemer-Avni, Y., Wallach, D. & Sarov, I. ( 1989; ). Reversion of the antichlamydial effect of tumor necrosis factor by tryptophan and antibodies to beta interferon. Infect Immun 57, 3484–3490.
     [Google Scholar]
  46. Shen, L., Shi, Y., Douglas, A. L., Hatch, T. P., O'Connell, C. M., Chen, J. M. & Zhang, Y.-X. ( 2000; ). Identification and characterization of promoters regulating tuf expression in Chlamydia trachomatis serovar F. Arch Biochem Biophys 379, 46–56.[CrossRef]
    [Google Scholar]
  47. Stephens, R. S. ( 1999; ). Genomic autobiographies of chlamydiae. In Chlamydia: Intracellular Biology, Pathogenesis and Immunity, pp. 9–27. Edited by R. S. Stephens. Washington, DC: American Society for Microbiology.
  48. Stephens, R. S., Kalman, S., Lammel, C. & 9 other authors ( 1998; ). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754–759.[CrossRef]
    [Google Scholar]
  49. Tan, M. & Engel, J. N. ( 1996; ). Identification of sequences necessary for transcription in vitro from the Chlamydia trachomatis rRNA P1 promoter. J Bacteriol 178, 6975–6982.
     [Google Scholar]
  50. Tan, M., Wong, B. & Engel, J. N. ( 1996; ). Transcriptional organization and regulation of the dnaK and groE operons of Chlamydia trachomatis. J Bacteriol 178, 6983–6990.
     [Google Scholar]
  51. Tomoyasu, T., Ohkishi, T., Ukyo, Y. & 7 other authors ( 2002; ). The ClpXP ATP-dependent protease regulates flagellum synthesis in Salmonella enterica serovar typhimurium. J Bacteriol 184, 645–653.[CrossRef]
    [Google Scholar]
  52. Vicente, M., Chater, K. F. & De Lorenzo, V. ( 1999; ). Bacterial transcription factors involved in global regulation. Mol Microbiol 33, 8–17.[CrossRef]
    [Google Scholar]
  53. Wilson, A. C. & Tan, M. ( 2002; ). Functional analysis of the heat shock regulator HrcA of Chlamydia trachomatis. J Bacteriol 184, 6566–6571.[CrossRef]
    [Google Scholar]
  54. Yu, H. H. Y. & Tan, M. ( 2003; ). Sigma 28 RNA polymerase regulates hctB, a late developmental gene in Chlamydia. Mol Microbiol 50, 577–584.[CrossRef]
    [Google Scholar]
  55. Yura, T. & Nakahigashi, K. ( 1999; ). Regulation of the heat-shock response. Curr Opin Microbiol 2, 153–158.[CrossRef]
    [Google Scholar]
  56. Zhang, Y.-X., Shi, Y., Zhou, M. & Petsko, G. A. ( 1994; ). Cloning, sequencing, and expression in Escherichia coli of the gene encoding a 45-kilodalton protein, elongation factor Tu, from Chlamydia trachomatis serovar F. J Bacteriol 176, 1184–1187.
     [Google Scholar]
  57. Zhang, Y.-X., Tao, J., Zhou, M., Meng, Q., Zhang, L., Shen, L., Klein, R. & Miller, D. L. ( 1997; ). Elongation factor Ts of Chlamydia trachomatis: structure of the gene and properties of the protein. Arch Biochem Biophys 344, 43–52.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26734-0
Loading
Chlamydia trachomatisσ28 recognizes the fliC promoter of Escherichia coli and responds to heat shock in chlamydiae
Microbiology 150, 205 (2004); https://doi.org/10.1099/mic.0.26734-0
/content/journal/micro/10.1099/mic.0.26734-0
/content/journal/micro/10.1099/mic.0.26734-0
Loading

Data & Media loading...

Most Cited This Month

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