1887

Microbiology Society logo

Volume 147, Issue 9

Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in

The GenBank accession numbers for the sequences reported in this paper are AF128845 () and AF149031 ().

Free

Abstract

Hybridization to a PCR product derived from conserved sigma-factor sequences led to the identification of two DNA segments that display significant sequence similarity to the family of genes encoding the σ (RpoH) heat-shock transcription factors. The first gene, , complements an mutation. Cells containing an mutation are impaired in growth at 37 °C under free-living conditions and are defective in nitrogen fixation during symbiosis with alfalfa. A plasmid-borne fusion increases in expression upon entry of the culture into the stationary phase of growth. The second gene, designated , is 42% identical to the gene. Cells containing an mutation have no apparent phenotype under free-living conditions or during symbiosis with the host plant alfalfa. An fusion increases in expression during the stationary phase of growth. The presence of two -like sequences in is reminiscent of the situation in , which has three genes.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): sigma-32 , stress , symbiosis and transcription factor
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-9-2399
2001-09-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/9/1472399a.html?itemId=/content/journal/micro/10.1099/00221287-147-9-2399&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Zhang J., Zheng Z., Miller W., Lipman D. J., Schäffer A. A. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  2. Arsène F., Tomoyasu T., Mogk A., Schirra C., Schulze-Specking A., Bukau B. 1999; Role of region C in regulation of the heat shock gene-specific sigma factor of Escherichia coli . J Bacteriol 181:3552–3561
     [Google Scholar]
  3. Babst M., Hennecke H., Fischer H.-M. 1996; Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum . Mol Microbiol 19:827–839 [CrossRef]
     [Google Scholar]
  4. Barnett M. J., Oke V., Long S. R. 2000; New genetic tools for use in the Rhizobiaceae and other bacteria. BioTechniques 29:240–245
     [Google Scholar]
  5. Beck C., Marty R., Hennecke H., Kläusli S., Göttfert M. 1997; Dissection of the transcription machinery for housekeeping genes of Bradyrhizobium japonicum . J Bacteriol 179:364–369
     [Google Scholar]
  6. Bent A. F., Signer E. R. 1990; Rhizobium meliloti suhR suppresses the phenotype of an Escherichia coli RNA polymerase σ32 mutant. J Bacteriol 172:3559–3568
     [Google Scholar]
  7. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. 1977; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95–113 [CrossRef]
     [Google Scholar]
  8. Bukau B. 1993; Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9:671–680 [CrossRef]
     [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395 [CrossRef]
     [Google Scholar]
  10. Erickson J. W., Vaughn V., Walter W. A., Neidhardt F. C., Gross C. A. 1987; Regulation of the promoters and transcripts of rpoH , the Escherichia coli heat shock regulatory gene. Genes Dev 1:419–432 [CrossRef]
     [Google Scholar]
  11. Finan T. M., Kunkel B., De Vos G. F., Signer E. R. 1986; Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167:66–72
     [Google Scholar]
  12. Galibert F., Finan T. M., Long S. R. 53 other authors 2001; The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672
     [Google Scholar]
  13. Gamer J., Multhaup G., Tomoyasu T., McCarty J. S., Schirra C., Bujard H., Bukau B., Rüdiger S., Schönfeld H.-J. 1996; A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates the activity of the Escherichia coli heat shock transcription factor σ32. EMBO J 15:607–617
     [Google Scholar]
  14. Gay P., Le Coq D., Steinmetz M., Berkelman T., Kado C. I. 1985; Positive selection procedure for entrapment of insertion sequence elements in Gram-negative bacteria. J Bacteriol 164:918–921
     [Google Scholar]
  15. Georgopoulos C., Liberek K., Zylicz M., Ang D. 1994; Properties of the heat shock proteins of Escherichia coli and the autoregulation of the heat shock response. In The Biology of Heat Shock Proteins and Molecular Chaperones pp 202–249 Edited by Morimoto R. I., Georgopoulos C., Tissières A. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  16. Glazebrook J., Walker G. C. 1991; Genetic techniques in Rhizobium meliloti. Methods Enzymol 204:398–418
     [Google Scholar]
  17. Gross C. A. 1996; Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 1382–1399 Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  18. Hecker M., Schumann W., Völker U. 1996; Heat-shock and general stress response in Bacillus subtilis . Mol Microbiol 19:417–428 [CrossRef]
     [Google Scholar]
  19. Herman C., d’Ari R., Bouloc P., Thévenet D. 1995; Degradation of σ32, the heat shock regulator in Escherichia coli , is governed by HflB. Proc Natl Acad Sci USA 92:3516–3520 [CrossRef]
     [Google Scholar]
  20. Jenkins D. E., Auger E. A., Matin A. 1991; Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J Bacteriol 173:1992–1996
     [Google Scholar]
  21. Joo D. M., Nolte A., Calendar R., Zhou Y. N., Jin D. J. 1998; Multiple regions on the Escherichia coli heat shock transcription factor σ32 determine core RNA polymerase binding specificity. J Bacteriol 180:1095–1102
     [Google Scholar]
  22. Kalinowski G., Long S. R. 1996; Deletion analysis of the 5′ untranslated region of the Rhizobium meliloti nodF gene. Mol Plant–Microbe Interact 9:869–873 [CrossRef]
     [Google Scholar]
  23. Kitagawa M., Wada C., Yoshioka S., Yura T. 1991; Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli , is controlled by a heat shock σ factor (σ32). J Bacteriol 173:4247–4253
     [Google Scholar]
  24. Kullik I., Fritsche S., Knobel H., Sanjuan J., Hennecke H., Fischer H.-M. 1991; Bradyrhizobium japonicum has two differentially regulated, functional homologs of the σ54 gene ( rpoN ). J Bacteriol 173:1125–1138
     [Google Scholar]
  25. Lonetto M., Gribskov M., Gross C. A. 1992; The σ70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849
     [Google Scholar]
  26. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn 5 mutagenesis. J Bacteriol 149:114–122
     [Google Scholar]
  27. Morita M. T., Tanaka Y., Kodama T. S., Kyogoku Y., Yanagi H., Yura T. 1999; Translational induction of heat shock transcription factor σ32: evidence for a built-in RNA thermosensor. Genes Dev 13:655–665 [CrossRef]
     [Google Scholar]
  28. Myler P. J., Venkatarman G. M., Lodes M. J., Stuart K. D. 1994; A frequently amplified region in Leishmania contains a gene frequently conserved in prokaryotes and eukaryotes. Gene 148:187–193 [CrossRef]
     [Google Scholar]
  29. Nagai H., Yuzawa H., Yura T. 1991; Interplay of two cis-acting mRNA regions in translational control of σ32 synthesis during the heat shock response of Escherichia coli . Proc Natl Acad Sci USA 88:10515–10519 [CrossRef]
     [Google Scholar]
  30. Nagai H., Yuzawa H., Kanemori M., Yura T. 1994; A distinct segment of the σ32 polypeptide is involved in DnaK-mediated negative control of the heat shock response in Escherichia coli . Proc Natl Acad Sci USA 91:10280–10284 [CrossRef]
     [Google Scholar]
  31. Nakahigashi K., Yanagi H., Yura T. 1995; Isolation and sequence analysis of rpoH genes encoding σ32 homologs from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res 23:4383–4390
     [Google Scholar]
  32. Narberhaus F., Weiglhofer W., Fisher H.-M., Hennecke H. 1996; The Bradyrhizobium japonicum rpoH 1 gene encoding a σ32-like protein is part of a unique heat shock gene cluster together with groESL 1 and three small heat shock genes. J Bacteriol 178:5337–5346
     [Google Scholar]
  33. Narberhaus F., Krummenacher P., Fischer H.-M., Hennecke H. 1997; Three disparately regulated genes for σ32-like transcription factors in Bradyrhizobium japonicum . Mol Microbiol 24:93–104 [CrossRef]
     [Google Scholar]
  34. Narberhaus F., Kaser R., Nocker A., Hennecke H. 1998a; A novel DNA element that controls bacterial heat shock gene expression. Mol Microbiol 28:315–323 [CrossRef]
     [Google Scholar]
  35. Narberhaus F., Kowarik M., Beck C., Hennecke H. 1998b; Promoter selectivity of the Bradyrhizobium japonicum transcription factors in vivo and in vitro. J Bacteriol 180:2395–2401
     [Google Scholar]
  36. Nicolas F. J., Cayuela M., Martı́nez-Argudo I. M., Ruiz-Vazquez R. M. 1996; High mobility group I(Y)-like DNA-binding domains on a bacterial transcription factor. Proc Natl Acad Sci USA 93:6881–6885 [CrossRef]
     [Google Scholar]
  37. Oke V., Long S. R. 1999; Bacterial genes induced within the nodule during the Rhizobium –legume symbiosis. Mol Microbiol 32:837–850 [CrossRef]
     [Google Scholar]
  38. Ono Y., Mitsui H., Sato T., Minamisawa K. 2001; Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti. Mol Gen Genet. 264902–912 [CrossRef]
  39. Østerås M., Stanley J., Finan T. M. 1995; Identification of Rhizobium- specific intergenic mosaic elements within an essential two-component regulatory system of Rhizobium species. J Bacteriol 177:5485–5494
     [Google Scholar]
  40. Quandt J., Hynes M. F. 1993; Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127:15–21 [CrossRef]
     [Google Scholar]
  41. Raychaudhuri S., Conrad J., Hall B. G., Ofengand J. 1998; A pseudouridine synthase required for the formation of two universally conserved pseudouridines in ribosomal RNA is essential for normal growth of Escherichia coli. RNA 4:1407–1417 [CrossRef]
     [Google Scholar]
  42. Ronson C. W., Nixon B. T., Albright L. M., Ausubel F. M. 1987; Rhizobium meliloti ntrA ( rpoN ) gene is required for diverse metabolic functions. J Bacteriol 169:2424–2431
     [Google Scholar]
  43. Rushing B. G. 1995 Transcription factors in Rhizobium meliloti: characterization of the positive regulator NodD3 and two sigma subunits, SigA and SigB PhD thesis Stanford University;
     [Google Scholar]
  44. Rushing B. G., Long S. R. 1995; Cloning and characterization of the sigA gene encoding the major sigma subunit of Rhizobium meliloti. J Bacteriol 177:6952–6957
     [Google Scholar]
  45. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  46. Squires C. L., Pedersen S., Ross B. M., Squires C. 1991; ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol 173:4254–4262
     [Google Scholar]
  47. Staskawicz B., Dahlbeck D., Keen N., Napoli C. 1987; Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol 169:5789–5794
     [Google Scholar]
  48. Straus D. B., Walter W. A., Gross C. A. 1987; The heat shock response of E. coli is regulated by changes in the concentration of σ32. Nature 329:348–351 [CrossRef]
     [Google Scholar]
  49. Swanson J. A., Mulligan J. T., Long S. R. 1993; Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics 134:435–444
     [Google Scholar]
  50. Thorne S. H., Williams H. D. 1997; Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance, and changes in macromolecular synthesis during entry to and exit from stationary phase. J Bacteriol 179:6894–6901
     [Google Scholar]
  51. Tilly K., Erickson J., Sharma S., Georgopoulos C. 1986; Heat shock regulatory gene rpoH mRNA level increases after heat shock in Escherichia coli . J Bacteriol 168:1155–1158
     [Google Scholar]
  52. Tilly K., Spence J., Georgopoulos C. 1989; Modulation of stability of the Escherichia coli heat shock regulatory factor σ32. J Bacteriol 171:1585–1589
     [Google Scholar]
  53. Tomoyasu T., Gamer J., Bukau B. 9 other authors 1995; Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor σ32. EMBO J 14:2551–2560
     [Google Scholar]
  54. Vieira J., Messing J. 1987; Production of single-stranded plasmid DNA. Methods Enzymol 153:3–11
     [Google Scholar]
  55. Wösten M. M. S. M. 1998; Eubacterial sigma-factors. FEMS Microbiol Rev 22:127–150 [CrossRef]
     [Google Scholar]
  56. Yura T. 1996; Regulation and conservation of the heat-shock transcription factor σ32. Genes Cells 1:277–284 [CrossRef]
     [Google Scholar]
  57. Yuzawa H., Nagai H., Mori H., Yura T. 1993; Heat induction of σ32 synthesis mediated by mRNA secondary structure: a primary step of the heat shock response in Escherichia coli . Nucleic Acids Res 21:5449–5455 [CrossRef]
     [Google Scholar]
  58. Zhou Y.-N., Kusukawa N., Erickson J. W., Gross C. A., Yura T. 1988; Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor σ32. J Bacteriol 170:3640–3649
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-9-2399
Loading
Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium melilotiThe GenBank accession numbers for the sequences reported in this paper are AF128845 (rpoH1) and AF149031 (rpoH2).
Microbiology 147, 2399 (2001); https://doi.org/10.1099/00221287-147-9-2399
/content/journal/micro/10.1099/00221287-147-9-2399
/content/journal/micro/10.1099/00221287-147-9-2399
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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