This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ma, Z.
Right arrow Articles by Foster, J. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ma, Z.
Right arrow Articles by Foster, J. W.

 Previous Article  |  Next Article 

Journal of Bacteriology, December 2002, p. 7001-7012, Vol. 184, No. 24
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.24.7001-7012.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Collaborative Regulation of Escherichia coli Glutamate-Dependent Acid Resistance by Two AraC-Like Regulators, GadX and GadW (YhiW)

Zhuo Ma,1 Hope Richard,1 Don L. Tucker,2 Tyrrell Conway,2 and John W. Foster1*

Department of Microbiology and Immunology, University of South Alabama College of Medicine, Mobile, Alabama 36688,1 Department of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 730192

Received 18 July 2002/ Accepted 27 September 2002

An important feature of Escherichia coli pathogenesis is an ability to withstand extremely acidic environments of pH 2 or lower. This acid resistance property contributes to the low infectious dose of pathogenic E. coli species. One very efficient E. coli acid resistance system encompasses two isoforms of glutamate decarboxylase (gadA and gadB) and a putative glutamate:{gamma}-amino butyric acid (GABA) antiporter (gadC). The system is subject to complex controls that vary with growth media, growth phase, and growth pH. Previous work has revealed that the system is controlled by two sigma factors, two negative regulators (cyclic AMP receptor protein [CRP] and H-NS), and an AraC-like regulator called GadX. Earlier evidence suggested that the GadX protein acts both as a positive and negative regulator of the gadA and gadBC genes depending on environmental conditions. New data clarify this finding, revealing a collaborative regulation between GadX and another AraC-like regulator called GadW (previously YhiW). GadX and GadW are DNA binding proteins that form homodimers in vivo and are 42% homologous to each other. GadX activates expression of gadA and gadBC at any pH, while GadW inhibits GadX-dependent activation. Regulation of gadA and gadBC by either regulator requires an upstream, 20-bp GAD box sequence. Northern blot analysis further indicates that GadW represses expression of gadX. The results suggest a control circuit whereby GadW interacts with both the gadA and gadX promoters. GadW clearly represses gadX and, in situations where GadX is missing, activates gadA and gadBC. GadX, however, activates only gadA and gadBC expression. CRP also represses gadX expression. It does this primarily by repressing production of sigma S, the sigma factor responsible for gadX expression. In fact, the acid induction of gadA and gadBC observed when rich-medium cultures enter stationary phase corresponds to the acid induction of sigma S production. These complex control circuits impose tight rein over expression of the gadA and gadBC system yet provide flexibility for inducing acid resistance under many conditions that presage acid stress.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, University of South Alabama College of Medicine, Mobile, AL 36688. Phone: (251) 460-6323. Fax: (251) 460-7931. E-mail: fosterj{at}sungcg.usouthal.edu.

Journal of Bacteriology, December 2002, p. 7001-7012, Vol. 184, No. 24
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.24.7001-7012.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Bergholz, T. M., Tarr, C. L., Christensen, L. M., Betting, D. J., Whittam, T. S. (2007). Recent Gene Conversions between Duplicated Glutamate Decarboxylase Genes (gadA and gadB) in Pathogenic Escherichia coli. Mol Biol Evol 24: 2323-2333 [Abstract] [Full Text]  
  • Richard, H., Foster, J. W. (2007). Sodium regulates Escherichia coli acid resistance, and influences GadX- and GadW-dependent activation of gadE. Microbiology 153: 3154-3161 [Abstract] [Full Text]  
  • Sayed, A. K., Odom, C., Foster, J. W. (2007). The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153: 2584-2592 [Abstract] [Full Text]  
  • Mates, A. K., Sayed, A. K., Foster, J. W. (2007). Products of the Escherichia coli Acid Fitness Island Attenuate Metabolite Stress at Extremely Low pH and Mediate a Cell Density-Dependent Acid Resistance. J. Bacteriol. 189: 2759-2768 [Abstract] [Full Text]  
  • Castanie-Cornet, M.-P., Treffandier, H., Francez-Charlot, A., Gutierrez, C., Cam, K. (2007). The glutamate-dependent acid resistance system in Escherichia coli: essential and dual role of the His-Asp phosphorelay RcsCDB/AF. Microbiology 153: 238-246 [Abstract] [Full Text]  
  • 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. Bacteriol. 188: 8118-8127 [Abstract] [Full Text]  
  • Bhagwat, A. A., Chan, L., Han, R., Tan, J., Kothary, M., Jean-Gilles, J., Tall, B. D. (2005). Characterization of Enterohemorrhagic Escherichia coli Strains Based on Acid Resistance Phenotypes. Infect. Immun. 73: 4993-5003 [Abstract] [Full Text]  
  • Stewart, N., Feng, J., Liu, X., Chaudhuri, D., Foster, J. W., Drolet, M., Tse-Dinh, Y.-C. (2005). Loss of topoisomerase I function affects the RpoS-dependent and GAD systems of acid resistance in Escherichia coli. Microbiology 151: 2783-2791 [Abstract] [Full Text]  
  • 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. Chem. 280: 21498-21505 [Abstract] [Full Text]  
  • Salmon, K. A., Hung, S.-p., Steffen, N. R., Krupp, R., Baldi, P., Hatfield, G. W., Gunsalus, R. P. (2005). Global Gene Expression Profiling in Escherichia coli K12: EFFECTS OF OXYGEN AVAILABILITY AND ArcA. J. Biol. Chem. 280: 15084-15096 [Abstract] [Full Text]  
  • Weber, H., Polen, T., Heuveling, J., Wendisch, V. F., Hengge, R. (2005). Genome-Wide Analysis of the General Stress Response Network in Escherichia coli: {sigma}S-Dependent Genes, Promoters, and Sigma Factor Selectivity. J. Bacteriol. 187: 1591-1603 [Abstract] [Full Text]  
  • Zwir, I., Shin, D., Kato, A., Nishino, K., Latifi, T., Solomon, F., Hare, J. M., Huang, H., Groisman, E. A. (2005). Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc. Natl. Acad. Sci. USA 102: 2862-2867 [Abstract] [Full Text]  
  • Maurer, L. M., Yohannes, E., Bondurant, S. S., Radmacher, M., Slonczewski, J. L. (2005). pH Regulates Genes for Flagellar Motility, Catabolism, and Oxidative Stress in Escherichia coli K-12. J. Bacteriol. 187: 304-319 [Abstract] [Full Text]  
  • 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. Bacteriol. 186: 7378-7389 [Abstract] [Full Text]  
  • Opdyke, J. A., Kang, J.-G., Storz, G. (2004). GadY, a Small-RNA Regulator of Acid Response Genes in Escherichia coli. J. Bacteriol. 186: 6698-6705 [Abstract] [Full Text]  
  • 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. Microbiol. 70: 4792-4799 [Abstract] [Full Text]  
  • Yohannes, E., Barnhart, D. M., Slonczewski, J. L. (2004). pH-Dependent Catabolic Protein Expression during Anaerobic Growth of Escherichia coli K-12. J. Bacteriol. 186: 192-199 [Abstract] [Full Text]  
  • 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. Microbiology 150: 61-72 [Abstract] [Full Text]  
  • Ma, Z., Richard, H., Foster, J. W. (2003). 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. Bacteriol. 185: 6852-6859 [Abstract] [Full Text]  
  • Iyer, R., Williams, C., Miller, C. (2003). Arginine-Agmatine Antiporter in Extreme Acid Resistance in Escherichia coli. J. Bacteriol. 185: 6556-6561 [Abstract] [Full Text]  
  • 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. Bacteriol. 185: 4402-4409 [Abstract] [Full Text]  
  • Waterman, S. R., Small, P. L. C. (2003). Transcriptional Expression of Escherichia coli Glutamate-Dependent Acid Resistance Genes gadA and gadBC in an hns rpoS Mutant. J. Bacteriol. 185: 4644-4647 [Abstract] [Full Text]  
  • Ruiz, R., Marques, S., Ramos, J. L. (2003). Leucines 193 and 194 at the N-Terminal Domain of the XylS Protein, the Positive Transcriptional Regulator of the TOL meta-Cleavage Pathway, Are Involved in Dimerization. J. Bacteriol. 185: 3036-3041 [Abstract] [Full Text]  
  • 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. Bacteriol. 185: 3190-3201 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»