1887

Abstract

The starvation-stress response (SSR) of includes gene products necessary for starvation avoidance, starvation survival and virulence for this bacterium. Numerous genetic loci induced during carbon-source starvation and required for the long-term-starvation survival of this bacterium have been identified. The SSR not only protects the cell against the adverse effects of long-term starvation but also provides cross-resistance to other environmental stresses, e.g. thermal challenge (55 °C) or acid-pH challenge (pH 28). One carbon-starvation-inducible fusion, designated was previously reported to be a σ-dependent SSR locus that is phosphate-starvation, nitrogen-starvation and HO inducible, positively regulated by (p)ppGpp in a -dependent manner, and negatively regulated by cAMP:cAMP receptor protein complex and OxyR. We have discovered through sequence analysis and subsequent biochemical analysis that the :: fusion, and a similarly regulated fusion designated , lie at separate sites within the first gene () of an operon encoding a cryptic nitrate reductase () of unknown physiological function. In this study, it was demonstrated that was negatively regulated by the global regulator Fnr during anaerobiosis. Interestingly, ) was required for carbon-starvation-inducible thermotolerance and acid tolerance. In addition, expression was induced ∼20-fold intracellularly in Madin-Darby canine kidney epithelial cells and ∼16-fold in intracellular salts medium, which is believed to mimic the intracellular milieu. Also, a knock-out mutation increased the LD ∼10-fold for SL1344 delivered orally in the mouse virulence model. Thus, the previously believed cryptic and constitutive operon is in fact highly regulated by a complex network of environmental-stress signals and global regulatory functions, indicating a central role in the physiology of starved and stressed cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-145-11-3035
1999-11-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/145/11/1453035a.html?itemId=/content/journal/micro/10.1099/00221287-145-11-3035&mimeType=html&fmt=ahah

References

  1. Archer C. D., Wang X., Elliott T. 1993; Mutants defective in the energy-conserving NADH dehydrogenase of Salmonella typhimurium identified by a decrease in energy-dependent proteolysis after carbon starvation. Proc Natl Acad Sci USA 90:9877–9881 [CrossRef]
    [Google Scholar]
  2. Atlung T., Knudsen K., Lotte H., Brøndsted L. 1997; Effects of σS and the transcriptional activator AppY on induction of the Escherichia colihya and cbdAB–appA operons in response to carbon and phosphate starvation. J Bacteriol 179:2141–2146
    [Google Scholar]
  3. Babior B. M. 1992; The respiratory burst oxidase. Adv Enzymol Relat Areas Mol Biol 65:49–95
    [Google Scholar]
  4. Barrett E. L., Riggs D. L. 1982; Evidence for a second nitrate reductase activity that is distinct from the respiratory enzyme in Salmonella typhimurium. J Bacteriol 150:563–571
    [Google Scholar]
  5. Blasco F., Iobbi C., Ratouchniak J., Bonnefoy V., Chippaux M. 1990; Nitrate reductases of Escherichia coli: sequence of the second nitrate reductase and comparison with that encoded by the narGHJI operon. Mol Gen Genet 222:104–111
    [Google Scholar]
  6. Bonnefoy V., DeMoss J. A. 1994; Nitrate reductases in Escherichia coli. Antonie Leeuwenhoek 66:47–56 [CrossRef]
    [Google Scholar]
  7. Brown M. R. W., Williams P. 1985; The influence of environment on envelope properties affecting survival of bacteria in infections. Annu Rev Microbiol 39:527–556 [CrossRef]
    [Google Scholar]
  8. Cashel M., Gentry D. R., Hernandez V. J., Vinella D. 1996; The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 1458–1496Edited by Neidhardt F. C. others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  9. Castilho B. A., Olfson P., Casadaban M. J. 1984; Plasmid insertion mutagenesis and lac gene fusions with mini-Mu bacteriophage transposons. J Bacteriol 158:488–495
    [Google Scholar]
  10. Chan R. K., Botstein D., Watanabe T., Ogata Y. 1972; Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high transducing lysate. Virology 50:883–898 [CrossRef]
    [Google Scholar]
  11. Davis R. W., Botstein D., Roth J. R. 1980 Advanced Bacterial Genetics Cold Spring Harbor NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  12. Dukan S., Nyström T. 1998; Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev 12:3431–3441 [CrossRef]
    [Google Scholar]
  13. Fang F. C., Libby S. J., Buchmeier N. A., Loewen P. C., Switala J., Harwood J., Guiney D. G. 1992; The alternative σ factor KatF (RpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA 89:11978–11982 [CrossRef]
    [Google Scholar]
  14. Finlay B. B., Falkow S. 1989; Salmonella as an intracellular parasite. Mol Microbiol 3:1833–1841 [CrossRef]
    [Google Scholar]
  15. Foster J. W., Spector M. P. 1986; Phosphate-starvation regulon of Salmonella typhimurium. J Bacteriol 166:666–669
    [Google Scholar]
  16. Foster J. W., Spector M. P. 1995; How Salmonella survive against the odds. Annu Rev Microbiol 49:145–174 [CrossRef]
    [Google Scholar]
  17. Garcia del Portillo F., Foster J. W., Maguire M. E., Finlay B. B. 1992; Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells. Mol Microbiol 6:3289–3297 [CrossRef]
    [Google Scholar]
  18. Gennis R. B., Stewart V. 1996; Respiration. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 217–261Edited by Neidhardt F C . others Washington DC: American Society for Microbiology;
    [Google Scholar]
  19. Goldman B. S., Gabbert K. K., Kranz R. G. 1996; The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178:6348–6351
    [Google Scholar]
  20. Harder W., Dijkhuizen L. 1983; Physiological responses to nutrient limitation. Annu Rev Microbiol 37:1–23 [CrossRef]
    [Google Scholar]
  21. Hengge-Aronis R. 1993; The role of rpoS in early stationary-phase gene regulation in Escherichia coli K12. In Starvation in Bacteria pp. 171–200Edited by Kjelleberg S. New York: Plenum;
    [Google Scholar]
  22. Hengge-Aronis R. 1996; Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 1497–1512Edited by Neidhardt F. C. others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Hoiseth S. K., Stocker B. A. D. 1981; Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238–239 [CrossRef]
    [Google Scholar]
  24. Iobbi-Nivol C., Santini C. L., Blasco F., Giordano G. 1990; Purification and further characterization of the second nitrate reductase of Escherichia coli K-12. Eur J Biochem 188:679–687 [CrossRef]
    [Google Scholar]
  25. Jenkins D. E., Schultz J. E., Matin A. 1988; Starvation-induced cross-protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol 170:3910–3914
    [Google Scholar]
  26. Koch A. L. 1971; The adaptive response of Escherichia coli to a feast and famine existence. Adv Microb Physiol 6:147–217
    [Google Scholar]
  27. Lange R., Hengge-Aronis R. 1991; Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5:49–59 [CrossRef]
    [Google Scholar]
  28. Lee I. S., Slonczewski J. L., Foster J. W. 1994; A low-pH inducible stationary-phase acid tolerance response in Salmonella typhimurium. J Bacteriol 176:1422–1426
    [Google Scholar]
  29. Loewen P. C., Hengge-Aronis R. 1994; The role of the sigma factor σS (KatF) in bacterial global regulation. Annu Rev Microbiol 48:53–80 [CrossRef]
    [Google Scholar]
  30. McCann M. P., Fraley C. D., Matin A. 1991; The putative σ factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol 173:4188–4194
    [Google Scholar]
  31. McLeod G. I., Spector M. P. 1996; Starvation- and stationary-phase-induced resistance to the antimicrobial peptide polymyxin B in Salmonella typhimurium is RpoS (σS) independent and occurs through both phoP-dependent and -independent pathways. J Bacteriol 178:3683–3688
    [Google Scholar]
  32. Mahan M. J., Tobias J. W., Slauch J. M., Hanna P. C., Collier J. R., Mekalanos J. J. 1995; Antibiotic based selection for bacterial genes that are specifically induced during infection of a host. Proc Natl Acad Sci USA 92:669–673 [CrossRef]
    [Google Scholar]
  33. Maloy S. R. 1990 Experimental Techniques in Bacterial Genetics Boston, MA: Jones & Bartlett;
    [Google Scholar]
  34. Matin A. 1991; The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 5:3–10 [CrossRef]
    [Google Scholar]
  35. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. 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;
    [Google Scholar]
  37. Moriarty D. J. W., Bell R. T. 1993; Bacterial growth and starvation in aquatic environments. In Starvation in Bacteria pp. 25–53Edited by Kjelleberg S. New York: Plenum;
    [Google Scholar]
  38. Morita R. Y. 1988; Bioavailability of energy and its relationship to growth and starvation survival in nature. Can J Microbiol 34:436–441 [CrossRef]
    [Google Scholar]
  39. Mulvey M. R., Loewen P. C. 1989; Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel σ transcription factor. Nucleic Acids Res 17:9979–9991 [CrossRef]
    [Google Scholar]
  40. Neidhardt F. C., Bloch P. L., Smith D. F. 1974; Culture medium for enterobacteria. J Bacteriol 119:736–747
    [Google Scholar]
  41. Nyström T., Larsson C., Gustafsson L. 1996; Bacterial defense against aging: role of the Escherichia coli ArcA regulator in gene expression, readjusted energy flux and survival during stasis. EMBO J 15:3219–3228
    [Google Scholar]
  42. O’Neal C. R., Gabriel W. M., Turk A. K., Libby S. J., Fang F. C., Spector M. P. 1994; RpoS is necessary for both the positive and negative regulation of starvation survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium. J Bacteriol 176:4610–4616
    [Google Scholar]
  43. Parks C. L, Chang L. S., Shenk T. 1991; A polymerase chain reaction mediated by a single primer: cloning of genomic sequences adjacent to a serotonin receptor protein coding region. Nucleic Acids Res 19:7155–7160 [CrossRef]
    [Google Scholar]
  44. Rosenthal A., Coutelle O., Craxton M. 1993; Large-scale production of DNA sequencing template by microtitre format PCR. Nucleic Acids Res 21:173–174 [CrossRef]
    [Google Scholar]
  45. Roszak D. B., Colwell R. R. 1987; Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379
    [Google Scholar]
  46. Seymour R. L., Mishra P. V., Khan M. A., Spector M. P. 1996; Essential roles of core starvation-stress response loci in carbon-starvation-inducible cross-resistance and hydrogen peroxide-inducible adaptive resistance to oxidative challenge in Salmonella typhimurium. Mol Microbiol 20:497–505 [CrossRef]
    [Google Scholar]
  47. Spector M. P. 1990; Gene expression in response to multiple nutrient-starvation conditions in Salmonella typhimurium. FEMS Microbiol Ecol 74:175–184 [CrossRef]
    [Google Scholar]
  48. Spector M. P. 1998; The starvation-stress response (SSR) of Salmonella. Adv Microb Physiol 40:233–279
    [Google Scholar]
  49. Spector M. P., Cubitt C. L. 1992; Starvation-inducible loci of Salmonella typhimurium: regulation and roles in starvation survival. Mol Microbiol 6:1467–1476 [CrossRef]
    [Google Scholar]
  50. Spector M. P., Foster J. W. 1993; Starvation-stress response (SSR) of Salmonella typhimurium: gene expression and survival during nutrient starvation. In Starvation in Bacteria pp. 201–224Edited by Kjelleberg S. New York: Plenum;
    [Google Scholar]
  51. Spector M. P., Aliabadi Z., Gonzalez T., Foster J. W. 1986; Global control in Salmonella typhimurium: two-dimensional gel electrophoretic analysis of starvation-, anaerobiosis-, and heat-shock-inducible proteins. J Bacteriol 168:420–424
    [Google Scholar]
  52. Spector M. P., Park Y. K., Tirgari S., Gonzalez T., Foster J. W. 1988; Identification and characterization of starvation-regulated genetic loci in Salmonella typhimurium by using Mud-directed lacZ operon fusions. J Bacteriol 170:345–351
    [Google Scholar]
  53. Spector M. P., DiRusso C. C., Pallen M. J., Garcia del Portillo F., Dougan G., Finlay B. B. 1999; The medium-/long-chain fatty acyl-CoA dehydrogenase (fadF) gene of Salmonella typhimurium is a phase 1 starvation-stress response (SSR) locus. Microbiology 145:15–31 [CrossRef]
    [Google Scholar]
  54. Storz G., Altuvia S. 1994; OxyR regulon. Methods Enzymol 234:217–223
    [Google Scholar]
  55. Storz G., Tartaglia L. A., Ames B. N. 1990; Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248:189–194 [CrossRef]
    [Google Scholar]
  56. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. 1993; Heterogeneity of the principal σ factor in Escherichia coli: the rpoS gene product, σ38, is a second principal σ factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci USA 90:3511–3515 [CrossRef]
    [Google Scholar]
  57. Valdivia R. H., Falkow S. 1997; Probing bacterial gene expression within host cells. Trends Microbiol 5:360–363 [CrossRef]
    [Google Scholar]
  58. Wall D., Delaney J. M., Fayet O., Lipinska B., Yamamoto T., Georgopoulos C. 1992; arcA-dependent thermal regulation and extragenic suppression of the Escherichia coli cytochrome d operon. J Bacteriol 174:6554–6562
    [Google Scholar]
  59. Way S. S., Sallustio S., Magliozzo R. S., Goldberg M. B. 1999; Impact of either increased or decreased levels of cytochrome bd expression on Shigella flexneri virulence. J Bacteriol 181:1229–1237
    [Google Scholar]
  60. Wilson J. A., Doyle T. J., Gulig P. A. 1997; Exponential-phase expression of spvA of the Salmonella typhimurium virulence plasmid: induction in intracellular salts medium and intracellularly in mice and cultured mammalian cells. Microbiology 143:3827–3839 [CrossRef]
    [Google Scholar]
  61. Zambrano M. M., Kolter R. 1993; Escherichia coli mutants lacking NADH dehydrogenase I have a competitive disadvantage in stationary phase. J Bacteriol 175:5642–5647
    [Google Scholar]
  62. Zambrano M. M., Siegele D. A., Almirón, M., Tormo A., Kolter R. 1993; Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757–1760 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/00221287-145-11-3035
Loading
/content/journal/micro/10.1099/00221287-145-11-3035
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