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
2019-12-08
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 coli hya 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. 1458–1496. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  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.
  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. 217–261. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  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. 171-200. Edited by S. Kjelleberg. New York: Plenum.
  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. 1497–1512. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  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.
  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.
  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.
  37. Moriarty, D. J. W. & Bell, R. T. ( 1993; ). Bacterial growth and starvation in aquatic environments. In Starvation in Bacteria, pp. 25-53. Edited by S. Kjelleberg. New York: Plenum.
  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. 201-224. Edited by S. Kjelleberg. New York: Plenum.
  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]
http://instance.metastore.ingenta.com/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