1887

Abstract

can survive pH 2 acid stress by using several acid resistance systems. The most efficient of these employs glutamate decarboxylase (GadA/GadB) to consume protons, and an antiporter (GadC) to exchange the intracellular decarboxylation product for external glutamic acid. Expression of the essential transcriptional activator of this system, GadE, is controlled by several regulators in a hierarchical fashion. In this study, two additional activators have been identified. The AraC-family regulators GadX and GadW, previously found to activate , are now shown to directly activate expression, which, in turn, activates the genes. results using and show that these regulators actually have little direct effect on and promoters. The numerous induction pathways converge on a 798 bp control region situated upstream of the promoter region. Deletions of this control region exposed the region between −798 and −360 nt (relative to the translational start) to be required for maximum expression in Luria–Bertani (LB) medium and to be the primary focus of GadX and GadW control. The GadE protein itself, which binds to three GAD box sequences present between −233 and −42 nt, helped activate GadE expression in LB, but only when the −798 to −360 region was absent. These regulatory regions and proteins appear to integrate a variety of physiological signals that forecast a need for GadE-dependent gene expression and acid resistance.

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2007-08-01
2020-08-04
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References

  1. Bordi C., Theraulaz L., Mejean V., Jourlin-Castelli C.. 2003; Anticipating an alkaline stress through the Tor phosphorelay system in Escherichia coli . Mol Microbiol48:211–223
    [Google Scholar]
  2. 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]
  3. Castanie-Cornet M. P., Penfound T. A., Smith D., Elliott J. F., Foster J. W.. 1999; Control of acid resistance in Escherichia coli . J Bacteriol181:3525–3535
    [Google Scholar]
  4. Castanie-Cornet M. P., Cam K., Jacq A.. 2006; RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli . J Bacteriol188:4264–4270
    [Google Scholar]
  5. Curtiss R., III., Porter S. B., Munson M., Tinge S. A., Hassan J. O., Gentry-Weeks C., Kelly S. M.. 1991; Nonrecombinant and recombinant avirulent Salmonella vaccines for poultry. In Colonization Control of Human Bacterial Enteropathogens in Poultry pp169–198 Edited by Blankenship L. C., Bailey J. H. S., Cox N. A., Stern N. J., Meinersmann R. J. New York: Academic Press;
  6. Dahan S., Knutton S., Shaw R. K., Crepin V. F., Dougan G., Frankel G.. 2004; Transcriptome of enterohemorrhagic Escherichia coli O157 adhering to eukaryotic plasma membranes. Infect Immun72:5452–5459
    [Google Scholar]
  7. De Biase D., Tramonti A., Bossa F., Visca P.. 1999; The response to stationary-phase stress conditions in Escherichia coli : role and regulation of the glutamic acid decarboxylase system. Mol Microbiol32:1198–1211
    [Google Scholar]
  8. Elliott T.. 1992; A method for constructing single-copy lac fusions in Salmonella typhimurium and its application to the hemA-prfA operon. J Bacteriol174:245–253
    [Google Scholar]
  9. Foster J. W.. 2004; Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol2:898–907
    [Google Scholar]
  10. Giangrossi M., Zattoni S., Tramonti A., De Biase D., Falconi M.. 2005; Antagonistic role of H-NS and GadX in the regulation of the glutamate decarboxylase-dependent acid resistance system in Escherichia coli . J Biol Chem280:21498–21505
    [Google Scholar]
  11. Giannella R. A., Broitman S. A., Zamcheck N.. 1973; Influence of gastric acidity on bacterial and parasitic enteric infections. A perspective. Ann Intern Med78:271–276
    [Google Scholar]
  12. Gong S., Richard H., Foster J. W.. 2003; YjdE (AdiC) is the arginine: agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli . J Bacteriol185:4402–4409
    [Google Scholar]
  13. Gong S., Ma Z., Foster J. W.. 2004; The Era-like GTPase TrmE conditionally activates gadE and glutamate-dependent acid resistance in Escherichia coli . Mol Microbiol54:948–961
    [Google Scholar]
  14. Gorden J., Small P. L. C.. 1993; Acid resistance in enteric bacteria. Infect Immun61:364–367
    [Google Scholar]
  15. Guzman L.-M., Belin D., Carson M. J., Beckwith J.. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol177:4121–4130
    [Google Scholar]
  16. Hommais F., Krin E., Laurent-Winter C., Soutourina O., Malpertuy A., Le Caer J. P., Danchin A., Bertin P.. 2001; Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol40:20–36
    [Google Scholar]
  17. Hommais F., Krin E., Coppee J. Y., Lacroix C., Yeramian E., Danchin A., Bertin P.. 2004; GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli . Microbiology150:61–72
    [Google Scholar]
  18. Iyer R., Williams C., Miller C.. 2003; Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli . J Bacteriol185:6556–6561
    [Google Scholar]
  19. Lin J., Lee I. S., Frey J., Slonczewski J. L., Foster J. W.. 1995; Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri and Escherichia coli . J Bacteriol177:4097–4104
    [Google Scholar]
  20. Lin J., Smith M. P., Chapin K. C., Baik H. S., Bennett G. N., Foster J. W.. 1996; Mechanisms of acid resistance in enterohemorrhagic Escherichia coli . Appl Environ Microbiol62:3094–3100
    [Google Scholar]
  21. Ma Z., Richard H., Tucker D. L., Conway T., Foster J. W.. 2002; Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators. GadX and GadW (YhiW). J Bacteriol184:7001–7012
    [Google Scholar]
  22. Ma Z., Richard H., Foster J. W.. 2003a; pH-dependent modulation of cyclic AMP levels and GadW-dependent repression of RpoS affect synthesis of the GadX regulator and Escherichia coli acid resistance. J Bacteriol185:6852–6859
    [Google Scholar]
  23. Ma Z., Gong S., Richard H., Tucker D. L., Conway T., Foster J. W.. 2003b; GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol49:1309–1320
    [Google Scholar]
  24. Ma Z., Masuda N., Foster J. W.. 2004; Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli . J Bacteriol186:7378–7389
    [Google Scholar]
  25. Masuda N., Church G. M.. 2002; Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol184:6225–6234
    [Google Scholar]
  26. Masuda N., Church G. M.. 2003; Regulatory network of acid resistance genes in Escherichia coli . Mol Microbiol48:699–712
    [Google Scholar]
  27. 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;
  28. Opdyke J. A., Kang J. G., Storz G.. 2004; GadY, a small-RNA regulator of acid response genes in Escherichia coli . J Bacteriol186:6698–6705
    [Google Scholar]
  29. Price S. B., Wright J. C., DeGraves F. J., Castanie-Cornet M. P., Foster J. W.. 2004; Acid resistance systems required for survival of Escherichia coli O157 : H7 in the bovine gastrointestinal tract and in apple cider are different. Appl Environ Microbiol70:4792–4799
    [Google Scholar]
  30. Richard H. T., Foster J. W.. 2003; Acid resistance in Escherichia coli . Adv Appl Microbiol52:167–186
    [Google Scholar]
  31. Richard H., Foster J. W.. 2004; Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol186:6032–6041
    [Google Scholar]
  32. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  33. Shin S., Castanie-Cornet M. P., Foster J. W., Crawford J. A., Brinkley C., Kaper J. B.. 2001; An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol41:1133–1150
    [Google Scholar]
  34. Simons R. W., Houman F., Kleckner N.. 1987; Improved single and multicopy lac -based cloning vectors for protein and operon fusions. Gene53:85–96
    [Google Scholar]
  35. Smith J. L.. 2003; The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J Food Prot66:1292–1303
    [Google Scholar]
  36. Smith D. K., Kassam T., Singh B., Elliott J. F.. 1992; Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J Bacteriol174:5820–5826
    [Google Scholar]
  37. Tatsuno I., Nagano K., Taguchi K., Rong L., Mori H., Sasakawa C.. 2003; Increased adherence to Caco-2 cells caused by disruption of the yhiE and yhiF genes in enterohemorrhagic Escherichia coli O157 : H7. Infect Immun71:2598–2606
    [Google Scholar]
  38. Tramonti A., Visca P., De Canio M., Falconi M., De Biase D.. 2002; Functional characterization and regulation of gadX , a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. J Bacteriol184:2603–2613
    [Google Scholar]
  39. Tramonti A., De Canio M., Bossa F., De Biase D.. 2003; Stability and oligomerization of recombinant GadX, a transcriptional activator of the Escherichia coli glutamate decarboxylase system. Biochim Biophys Acta1647:376–380
    [Google Scholar]
  40. Tramonti A., De Canio M., Delany I., Scarlato V., De Biase D.. 2006; Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli . J Bacteriol188:8118–8127
    [Google Scholar]
  41. Tucker D. L., Tucker N., Conway T.. 2002; Gene expression profiling of the pH response in Escherichia coli . J Bacteriol184:6551–6558
    [Google Scholar]
  42. Tucker D. L., Tucker N., Ma Z., Foster J. W., Miranda R. L., Cohen P. S., Conway T.. 2003; Genes of the GadX-GadW regulon in Escherichia coli . J Bacteriol185:3190–3201
    [Google Scholar]
  43. Weber H., Polen T., Heuveling J., Wendisch V. F., Hengge R.. 2005; Genome-wide analysis of the general stress response network in Escherichia coli : sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol187:1591–1603
    [Google Scholar]
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