1887

Abstract

Carbon-energy source starvation is a commonly encountered stress that can influence the epidemiology and virulence of serovars. responds to C-starvation by eliciting the starvation-stress response (SSR), which allows for long-term C-starvation survival and cross-resistance to other stresses. The locus was identified as a C-starvation-inducible, -dependent locus required for a maximal SSR. We report here that the locus is an operon composed of the (putative transport protein) and (penicillin-binding protein-7/8) genes. transcription is initiated from a –dependent C-starvation-inducible promoter upstream of . Another ( -independent) promoter, upstream of , drives lower constitutive transcription, primarily during exponential phase. C-starvation-inducible expression was required for development of the SSR in 5 h, but not 24 h, C-starved cells; was dispensable for the SSR. Furthermore, the operon is induced within MDCK epithelial cells, but was not essential for oral virulence in BALB/c mice. Thus, PBP 7 is required for physiological changes, occurring within the first few hours of C-starvation, essential for the development of the SSR. Lack of PBP 7, however, can be compensated for by further physiological changes developed in 24 h C-starved cells. This supports the dynamic overlapping and distinct nature of resistance pathways within the SSR.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/005199-0
2007-07-01
2020-09-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/7/2148.html?itemId=/content/journal/micro/10.1099/mic.0.2007/005199-0&mimeType=html&fmt=ahah

References

  1. 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 defenses by enhancing σ S levels. Mol Microbiol56:811–823[CrossRef]
    [Google Scholar]
  2. Bébien M., Kirsch J., Méjean V., Verméglio A.. 2002; Involvement of a putative molybdenum enzyme in the reduction of selenate by Escherichia coli. Microbiology148:3865–3872
    [Google Scholar]
  3. Brown M. R. W., Williams P.. 1985; The influence of environment on envelope properties affecting survival of bacteria in infections. Annu Rev Microbiol39:527–556[CrossRef]
    [Google Scholar]
  4. Bullas L. R., Ryu J. I.. 1983; Salmonella typhimurium LT2 strains which are r m+ for all three chromosomally located systems of DNA restriction and modification. J Bacteriol156:471–474
    [Google Scholar]
  5. 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. Virology50:883–898[CrossRef]
    [Google Scholar]
  6. Datsenko K. A., Wanner B. L.. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645[CrossRef]
    [Google Scholar]
  7. Davis R. W., Botstein D., Roth J. R.. 1980; Advanced Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  8. Denome S. A., Elf P. K., Henderson T. A., Nelson D. E., Young K. D.. 1999; Escherichia coli mutants lacking all possible combinations of eight penicillin-binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J Bacteriol181:3981–3993
    [Google Scholar]
  9. Dougherty T. J., Pucci M. J.. 1994; Penicillin-binding proteins are regulated by rpoS during transitions in growth states of Escherichia coli. Antimicrob Agents Chemother38:205–210[CrossRef]
    [Google Scholar]
  10. 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 U S A89:11978–11982[CrossRef]
    [Google Scholar]
  11. Finlay B. B., Falkow S.. 1989; Salmonella as an intracellular parasite. Mol Microbiol3:1833–1841[CrossRef]
    [Google Scholar]
  12. Foster J. W., Spector M. P.. 1995; How Salmonella survive against the odds. Annu Rev Microbiol49:145–174[CrossRef]
    [Google Scholar]
  13. Franchini A. G., Egli T.. 2006; Global gene expression in Escherichia coli K-12 during short-term and long-term adaptation to glucose-limited continuous culture conditions. Microbiology152:2111–2127[CrossRef]
    [Google Scholar]
  14. 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 Microbiol6:3289–3297[CrossRef]
    [Google Scholar]
  15. Goffin C., Ghuysen J. M.. 2002; Biochemistry and comparative genomics of SxxK superfamily acyltransferases offer a clue to the mycobacterial paradox: presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent. Microbiol Mol Biol Rev66:702–738[CrossRef]
    [Google Scholar]
  16. Heidrich C., Ursinus A., Berger J., Schwartz H., Höltje J. V.. 2002; Effects of multiple deletions of murein hydrolases on viability, septum cleavage and sensitivity to large toxic molecules in Escherichia coli. J Bacteriol184:6093–6099[CrossRef]
    [Google Scholar]
  17. Henderson T. A., Dombrosky P. M., Young K. D.. 1994; Artifactual processing of penicillin-binding protein 7 and 1b by the OmpT protease of Escherichia coli. J Bacteriol176:256–259
    [Google Scholar]
  18. Henderson T. A., Templin M., Young K. D.. 1995; Identification and cloning of the gene encoding penicillin-binding protein 7 of Escherichia coli. J Bacteriol177:2074–2079
    [Google Scholar]
  19. Hoiseth S. K., Stocker B. A. D.. 1981; Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature291:238–239[CrossRef]
    [Google Scholar]
  20. Humphreys S., Stevenson A., Bacon A., Weinhardt A. B., Roberts M.. 1999; The alternative sigma factor, σ E, is critically important for the virulence of Salmonella typhimurium. Infect Immun67:1560–1568
    [Google Scholar]
  21. Jenkins D. E., Schultz J. E., Matin A.. 1988; Starvation-induced cross-protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol170:3910–3914
    [Google Scholar]
  22. Kazmierczak M. J., Weidman M., Boor K. J.. 2005; Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev69:527–543[CrossRef]
    [Google Scholar]
  23. Kenyon W. J., Sayers D. G., Humphreys S., Roberts M., Spector M. P.. 2002; The starvation-stress response of Salmonella enterica serovar Typhimurium requires σ E, but not CpxR-regulated, extracytoplasmic functions. Microbiology148:113–122
    [Google Scholar]
  24. Koch A. L.. 1971; The adaptive response of Escherichia coli to a feast and famine existence. Adv Microb Physiol6:147–217
    [Google Scholar]
  25. Kormanec J.. 2001; Analyzing the developmental expression of sigma factors with S1-nuclease mapping. Methods Mol Biol160:481–494
    [Google Scholar]
  26. Lacour S., Kolb A., Landini P.. 2003; Nucleotides from −16 to −12 determine specific promoter recognition by bacterial sigma S-RNA polymerase. J Biol Chem278:37160–37168[CrossRef]
    [Google Scholar]
  27. Loewen P. C., Hengge-Aronis R.. 1994; The role of the sigma factor σ S (KatF) in bacterial global regulation. Annu Rev Microbiol48:53–80[CrossRef]
    [Google Scholar]
  28. 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 U S A92:669–673[CrossRef]
    [Google Scholar]
  29. Maloy S. R.. 1989; Experimental Techniques in Bacterial Genetics Boston, MA: Jones & Bartlett;
    [Google Scholar]
  30. Maxam A. M., Gilbert W.. 1980; Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol65:499–560
    [Google Scholar]
  31. 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 Bacteriol173:4188–4194
    [Google Scholar]
  32. McLeod G. I., Spector M. P.. 1996; Starvation- and stationary-phase-induced resistance to the antimicrobial peptide polymyxin B in Salmonella typhimurium is RpoS ( σ S)-independent and occurs through both phoP -dependent and -independent pathways. J Bacteriol178:3683–3688
    [Google Scholar]
  33. Meberg B. M., Paulson A. L., Priyadarshini R., Young K. D.. 2004; Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in determining uniform morphology of Escherichia coli. J Bacteriol186:8326–8336[CrossRef]
    [Google Scholar]
  34. 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 Press;
    [Google Scholar]
  35. Moat A. G., Foster J. W., Spector M. P.. 2002; Microbial Physiology , 4th edn. New York, NY: John Wiley & Sons;
    [Google Scholar]
  36. Neidhardt F. C., Bloch P. L., Smith D. F.. 1974; Culture medium for enterobacteria. J Bacteriol119:736–747
    [Google Scholar]
  37. 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 Bacteriol176:4610–4616
    [Google Scholar]
  38. 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 Res19:7155–7160[CrossRef]
    [Google Scholar]
  39. Priyadarshini R., Popham D. L., Young K. D.. 2006; Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli. J Bacteriol188:5345–5355[CrossRef]
    [Google Scholar]
  40. Rezuchova B., Miticka H., Homerova D., Roberts M., Kormanec J.. 2003; New members of the Escherichia coli σ E regulon identified by a two-plasmid system. FEMS Microbiol Lett225:1–7[CrossRef]
    [Google Scholar]
  41. Romeis T., Höltje J. V.. 1994; Penicillin-binding protein 7/8 of Escherichia coli is a dd-endopeptidase. Eur J Biochem224:597–604[CrossRef]
    [Google Scholar]
  42. Rosenthal A., Coutelle O., Craxton M.. 1993; Large-scale production of DNA sequencing template by microtitre format PCR. Nucleic Acids Res21:173–174[CrossRef]
    [Google Scholar]
  43. Rowley G., Spector M., Kormanec J., Roberts M.. 2006; Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol4:383–394[CrossRef]
    [Google Scholar]
  44. Rozen Y., Belkin S.. 2001; Survival of enteric bacteria in seawater. FEMS Microbiol Rev25:513–529[CrossRef]
    [Google Scholar]
  45. 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 Microbiol20:497–505[CrossRef]
    [Google Scholar]
  46. Simons R. W., Houman F., Kleckner N.. 1987; Improved single and multicopy lac -based cloning vectors for protein and operon fusions. Gene53:85–96[CrossRef]
    [Google Scholar]
  47. Skovierova H., Rowley G., Rezuchova B., Homerova D., Lewis C., Roberts M., Kormanec J.. 2006; Identification of the σ E regulon of Salmonella enterica serovar Typhimurium. Microbiology152:1347–1359[CrossRef]
    [Google Scholar]
  48. Spector M. P.. 1990; Gene expression in response to multiple nutrient-starvation conditions in Salmonella typhimurium. FEMS Microbiol Ecol74:175–184[CrossRef]
    [Google Scholar]
  49. Spector M. P.. 1998; The starvation-stress response (SSR) of Salmonella. Adv Microb Physiol40:233–279
    [Google Scholar]
  50. Spector M. P., Cubitt C. L.. 1992; Starvation-inducible loci of Salmonella typhimurium : regulation and roles in starvation survival. Mol Microbiol6:1467–1476[CrossRef]
    [Google Scholar]
  51. 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 pp201–224 Edited by Kjelleberg S.. New York: Kluwer Academic/Plenum;
    [Google Scholar]
  52. 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 Bacteriol168:420–424
    [Google Scholar]
  53. 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 Bacteriol170:345–351
    [Google Scholar]
  54. Spector M. P., DiRusso C. C., Pallen M. J., Dougan G., Finlay B. B., Garcia del Portillo F.. 1999a; The medium-/long-chain fatty acyl-CoA dehydrogenase ( fadF ) gene of Salmonella typhimurium is a phase 1 starvation-stress response (SSR) locus. Microbiology145:15–31[CrossRef]
    [Google Scholar]
  55. Spector M. P., Bearson S. M., Mahmud A., Magut M., Finlay B. B., Dougan G., Foster J. W., Pallen M. J., Garcia del Portillo F.. 1999b; The rpoS -dependent starvation-stress response locus stiA encodes a nitrate reductase ( narZYWV ) required for carbon-starvation-inducible thermotolerance and acid tolerance in Salmonella typhimurium. Microbiology145:3035–3045
    [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, σ 38, is a second principal σ factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A90:3511–3515[CrossRef]
    [Google Scholar]
  57. Testerman T. L., Vazquez-Torres A., Xu Y., Jones-Carson J., Libby S. J., Fang F. C.. 2002; The alternative sigma factor σ E controls antioxidant defenses required for Salmonella virulence and stationary-phase survival. Mol Microbiol43:771–782[CrossRef]
    [Google Scholar]
  58. Tuomanen E., Cozens R.. 1987; Changes in peptidoglycan composition and penicillin-binding proteins in slowly growing Escherichia coli. J Bacteriol169:5308–5310
    [Google Scholar]
  59. Tuomanen E., Schwartz J.. 1987; Penicillin-binding protein 7 and its relationship to lysis of non-growing Escherichia coli. J Bacteriol169:4912–4915
    [Google Scholar]
  60. Typas A., Hengge R.. 2006; Role of the spacer between the −35 and −10 regions on σ S promoter selectivity in Escherichia coli. Mol Microbiol59:1037–1051[CrossRef]
    [Google Scholar]
  61. Valdivia R. H., Falkow S.. 1997; Probing bacterial gene expression within host cells. Trends Microbiol5:360–363[CrossRef]
    [Google Scholar]
  62. Weber H., Polen T., Heuveling J., Wendisch V. F., Hengge R.. 2005; Genome-wide analysis of the general stress response network in Escherichia coli : σ S-dependent genes, promoters, and sigma factor selectivity. J Bacteriol187:1591–1603[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/005199-0
Loading
/content/journal/micro/10.1099/mic.0.2007/005199-0
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