1887

Abstract

The physiological role and transcriptional expression of sigma factors and are reported in this work. Both and were able to complement the temperature-sensitive phenotype of an mutant. The mutant was sensitive to heat shock, sodium hypochlorite and hydrogen peroxide, whereas the mutant was sensitive to NaCl and sucrose. The double mutant had increased sensitivity to heat shock and oxidative stress when compared with the single mutant. This suggests that in , RpoH1 is the main heat-shock sigma factor, but a more complete protective response could be achieved with the participation of RpoH2. Conversely, RpoH2 is involved in osmotic tolerance. In symbiosis with bean plants, the and mutants still elicited nodule formation, but exhibited reduced nitrogenase activity and bacterial viability in early and late symbiosis compared with nodules produced by mutants and wild-type strains. In addition, nodules formed by and mutants showed premature senescence. It was also determined that and expression was affected in mutants. Both genes were induced under microaerobic conditions and in the stationary growth phase, but not in response to heat shock. Analysis of the upstream region of revealed a and a probable promoter, whereas in , one probable -dependent promoter was detected. In conclusion, the two RpoH proteins operate under different stress conditions, RpoH1 in heat-shock and oxidative responses, and RpoH2 in osmotic tolerance.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.021428-0
2009-02-01
2019-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/2/386.html?itemId=/content/journal/micro/10.1099/mic.0.021428-0&mimeType=html&fmt=ahah

References

  1. Arsène, F., Tomoyasu, T. & Bukau, B. ( 2000; ). The heat shock response of Escherichia coli. Int J Food Microbiol 55, 3–9.[CrossRef]
    [Google Scholar]
  2. Bang, I. S., Frye, J. G., McClelland, M., Velayudhan, J. & Fang, F. C. ( 2005; ). Alternative sigma factor interactions in Salmonella: σ E and σ H promote antioxidant defences by enhancing σ E levels. Mol Microbiol 56, 811–823.[CrossRef]
    [Google Scholar]
  3. Bittner, A. N. & Oke, V. ( 2006; ). Multiple groESL operons are not key targets of RpoH1 and RpoH2 in Sinorhizobium meliloti. J Bacteriol 188, 3507–3515.[CrossRef]
    [Google Scholar]
  4. Botsford, J. L. & Lewis, T. ( 1990; ). Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56, 488–494.
    [Google Scholar]
  5. Bravo, A. & Mora, J. ( 1988; ). Ammonium assimilation in Rhizobium phaseoli by the glutamine synthetase–glutamate synthase pathway. J Bacteriol 170, 980–984.
    [Google Scholar]
  6. Brewin, N. J. ( 1991; ). Development of the legume root nodule. Annu Rev Cell Biol 7, 191–226.[CrossRef]
    [Google Scholar]
  7. Davies, B. W. & Walker, G. C. ( 2007; ). Identification of novel Sinorhizobium meliloti mutants compromised for oxidative stress protection and symbiosis. J Bacteriol 189, 2110–2113.[CrossRef]
    [Google Scholar]
  8. Delory, M., Hallez, R., Letesson, J. J. & De Bolle, X. ( 2006; ). An RpoH-like heat shock sigma factor is involved in stress response and virulence in Brucella melitensis 16M. J Bacteriol 188, 7707–7710.[CrossRef]
    [Google Scholar]
  9. Díaz-Acosta, A., Sandoval, M. L., Delgado-Olivares, L. & Membrillo-Hernandez, J. ( 2006; ). Effect of anaerobic and stationary phase growth conditions on the heat shock and oxidative stress responses in Escherichia coli K-12. Arch Microbiol 185, 429–438.[CrossRef]
    [Google Scholar]
  10. Ditta, G., Stanfield, S., Corbin, D. & Helinski, D. R. ( 1980; ). Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A 77, 7347–7351.[CrossRef]
    [Google Scholar]
  11. Dombrecht, B., Heusdens, C., Beullens, S., Verreth, C., Mulkers, E., Proost, P., Vanderleyden, J. & Michiels, J. ( 2005; ). Defence of Rhizobium etli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin. Mol Microbiol 55, 1207–1221.[CrossRef]
    [Google Scholar]
  12. Domínguez-Ferreras, A., Pérez-Arnedo, R., Becker, A., Olivares, J., Soto, M. J. & Sanjuán, J. ( 2006; ). Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol 188, 7617–7625.[CrossRef]
    [Google Scholar]
  13. El-Samad, H., Kurata, H., Doyle, J. C., Gross, C. A. & Khammash, M. ( 2005; ). Surviving heat shock: control strategies for robustness and performance. Proc Natl Acad Sci U S A 102, 2736–2741.[CrossRef]
    [Google Scholar]
  14. 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]
  15. Fahraeus, G. ( 1957; ). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16, 374–381.[CrossRef]
    [Google Scholar]
  16. Fischer, H. M. ( 1994; ). Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58, 352–386.
    [Google Scholar]
  17. Galibert, F., Finan, T. M., Long, S. R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A. & other authors ( 2001; ). The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668–672.[CrossRef]
    [Google Scholar]
  18. Girard, L., Brom, S., Davalos, A., Lopez, O., Soberon, M. & Romero, D. ( 2000; ). Differential regulation of fixN-reiterated genes in Rhizobium etli by a novel fixL–fixK cascade. Mol Plant Microbe Interact 13, 1283–1292.[CrossRef]
    [Google Scholar]
  19. Gonzalez, V., Santamaria, R. I., Bustos, P., Hernández-González, I., Medrano-Soto, A., Moreno-Hagelsieb, G., Janga, S. C., Ramírez, M. A., Jiménez-Jacinto, V. & other authors ( 2006; ). The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci U S A 103, 3834–3839.[CrossRef]
    [Google Scholar]
  20. Green, H. A. & Donohue, T. J. ( 2006; ). Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. J Bacteriol 188, 5712–5721.[CrossRef]
    [Google Scholar]
  21. Gross, C. A. ( 1996; ). Function and regulation of the heat-shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, vol. 1, pp. 1382–1399. Edited by F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Rily, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
  22. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  23. Ishihama, A. ( 1997; ). Adaptation of gene expression in stationary phase bacteria. Curr Opin Genet Dev 7, 582–588.[CrossRef]
    [Google Scholar]
  24. Janaszak, A., Majczak, W., Nadratowska, B., Szalewska-Palasz, A., Konopa, G. & Taylor, A. ( 2007; ). A σ 54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene. Microbiology 153, 111–123.[CrossRef]
    [Google Scholar]
  25. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A. & other authors ( 2000; ). Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (Supplement). DNA Res 7, 381–406.[CrossRef]
    [Google Scholar]
  26. Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Idesawa, K., Iriguchi, M. & other authors ( 2002; ). Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9, 189–197.[CrossRef]
    [Google Scholar]
  27. Kaufusi, P. H., Forsberg, L. S., Tittabutr, P. & Borthakur, D. ( 2004; ). Regulation of exopolysaccharide synthesis in Rhizobium sp. strain TAL1145 involves an alternative sigma factor gene, rpoH2. Microbiology 150, 3473–3482.[CrossRef]
    [Google Scholar]
  28. Keen, N. T., Tamaki, S., Kobayashi, D. & Trollinger, D. ( 1988; ). Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70, 191–197.[CrossRef]
    [Google Scholar]
  29. Martínez-Salazar, J. M. & Romero, D. ( 2000; ). Role of the ruvB gene in homologous and homeologous recombination in Rhizobium etli. Gene 243, 125–131.[CrossRef]
    [Google Scholar]
  30. Metcalf, W. W. & Wanner, B. L. ( 1993; ). Construction of new β-glucuronidase cassettes for making transcriptional fusions and their use with new methods for allele replacement. Gene 129, 17–25.[CrossRef]
    [Google Scholar]
  31. Mitsui, H., Sato, T., Sato, Y., Ito, N. & Minamisawa, K. ( 2004; ). Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa. Mol Genet Genomics 271, 416–425.[CrossRef]
    [Google Scholar]
  32. Nakahigashi, K., Yanagi, H. & Yura, T. ( 1995; ). Isolation and sequence analysis of rpoH genes encoding σ 32 homologs from Gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res 23, 4383–4390.
    [Google Scholar]
  33. Narberhaus, F., Krummenacher, P., Fischer, H. M. & Hennecke, H. ( 1997; ). Three disparately regulated genes for σ 32-like transcription factors in Bradyrhizobium japonicum. Mol Microbiol 24, 93–104.[CrossRef]
    [Google Scholar]
  34. Noel, K. D., Sanchez, A., Fernandez, L., Leemans, J. & Cevallos, M. A. ( 1984; ). Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. J Bacteriol 158, 148–155.
    [Google Scholar]
  35. Nogales, J., Campos, R., BenAbdelkhalek, H., Olivares, J., Lluch, C. & Sanjuan, J. ( 2002; ). Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol Plant Microbe Interact 15, 225–232.[CrossRef]
    [Google Scholar]
  36. Nonaka, G., Blankschien, M., Herman, C., Gross, C. A. & Rhodius, V. A. ( 2006; ). Regulon and promoter analysis of the E. coli heat-shock factor, σ 32, reveals a multifaceted cellular response to heat stress. Genes Dev 20, 1776–1789.[CrossRef]
    [Google Scholar]
  37. Nystrom, T. ( 2004; ). Stationary-phase physiology. Annu Rev Microbiol 58, 161–181.[CrossRef]
    [Google Scholar]
  38. Oke, V., Rushing, B. G., Fisher, E. J., Moghadam-Tabrizi, M. & Long, S. R. ( 2001; ). Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti. Microbiology 147, 2399–2408.
    [Google Scholar]
  39. 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 264, 902–912.[CrossRef]
    [Google Scholar]
  40. Pichon, M., Journet, E. P., Dedieu, A., de Billy, F., Truchet, G. & Barker, D. G. ( 1992; ). Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4, 1199–1211.[CrossRef]
    [Google Scholar]
  41. Ramírez-Romero, M. A., Masulis, I., Cevallos, M. A., Gonzalez, V. & Davila, G. ( 2006; ). The Rhizobium etli σ 70 (SigA) factor recognizes a lax consensus promoter. Nucleic Acids Res 34, 1470–1480.[CrossRef]
    [Google Scholar]
  42. Romero, D., Singleton, P. W., Segovia, L., Morett, E., Bohlool, B. B., Palacios, R. & Davila, G. ( 1988; ). Effect of naturally occurring nif reiterations on symbiotic effectiveness in Rhizobium phaseoli. Appl Environ Microbiol 54, 848–850.
    [Google Scholar]
  43. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  44. Santos, R., Herouart, D., Sigaud, S., Touati, D. & Puppo, A. ( 2001; ). Oxidative burst in alfalfa–Sinorhizobium meliloti symbiotic interaction. Mol Plant Microbe Interact 14, 86–89.[CrossRef]
    [Google Scholar]
  45. Sauviac, L., Philippe, H., Phok, K. & Bruand, C. ( 2007; ). An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. J Bacteriol 189, 4204–4216.[CrossRef]
    [Google Scholar]
  46. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. & Puhler, A. ( 1994; ). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73.[CrossRef]
    [Google Scholar]
  47. Simon, R., Priefer, U. & Puhler, A. ( 1983; ). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology (N Y) 1, 784–791.[CrossRef]
    [Google Scholar]
  48. Taylor, W. E., Straus, D. B., Grossman, A. D., Burton, Z. F., Gross, C. A. & Burgess, R. R. ( 1984; ). Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38, 371–381.[CrossRef]
    [Google Scholar]
  49. 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]
  50. Tittabutr, P., Payakapong, W., Teaumroong, N., Boonkerd, N., Singleton, P. W. & Borthakur, D. ( 2006; ). The alternative sigma factor RpoH2 is required for salt tolerance in Sinorhizobium sp. strain BL3. Res Microbiol 157, 811–818.[CrossRef]
    [Google Scholar]
  51. Vento, R., Giuliano, M., Lauricella, M., Carabillo, M., Di Liberto, D. & Tesoriere, G. ( 1998; ). Induction of programmed cell death in human retinoblastoma Y79 cells by C2-ceramide. Mol Cell Biochem 185, 7–15.[CrossRef]
    [Google Scholar]
  52. Wösten, M. M. ( 1998; ). Eubacterial sigma-factors. FEMS Microbiol Rev 22, 127–150.[CrossRef]
    [Google Scholar]
  53. Yamamori, T. & Yura, T. ( 1980; ). Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J Bacteriol 142, 843–851.
    [Google Scholar]
  54. Yura, T., Nakahigashi, K. & Kanemori, M. ( 1996; ). Transcriptional regulation of stress-inducible genes in procaryotes. EXS 77, 165–181.
    [Google Scholar]
  55. Zahran, H. H. ( 1999; ). Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63, 968–989.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.021428-0
Loading
/content/journal/micro/10.1099/mic.0.021428-0
Loading

Data & Media loading...

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