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

pH-Dependent Expression of Periplasmic Proteins and Amino Acid Catabolism in Escherichia coli

Department of Biology, Kenyon College, Gambier, Ohio 43022

Received 12 February 2002/ Accepted 13 May 2002

Escherichia coli grows over a wide range of pHs (pH 4.4 to 9.2), and its own metabolism shifts the external pH toward either extreme, depending on available nutrients and electron acceptors. Responses to pH values across the growth range were examined through two-dimensional electrophoresis (2-D gels) of the proteome and through lac gene fusions. Strain W3110 was grown to early log phase in complex broth buffered at pH 4.9, 6.0, 8.0, or 9.1. 2-D gel analysis revealed the pH dependence of 19 proteins not previously known to be pH dependent. At low pH, several acetate-induced proteins were elevated (LuxS, Tpx, and YfiD), whereas acetate-repressed proteins were lowered (Pta, TnaA, DksA, AroK, and MalE). These responses could be mediated by the reuptake of acetate driven by changes in pH. The amplified proton gradient could also be responsible for the acid induction of the tricarboxylic acid (TCA) enzymes SucB and SucC. In addition to the autoinducer LuxS, low pH induced another potential autoinducer component, the LuxH homolog RibB. pH modulated the expression of several periplasmic and outer membrane proteins: acid induced YcdO and YdiY; base induced OmpA, MalE, and YceI; and either acid or base induced OmpX relative to pH 7. Two pH-dependent periplasmic proteins were redox modulators: Tpx (acid-induced) and DsbA (base-induced). The locus alx, induced in extreme base, was identified as ygjT, whose product is a putative membrane-bound redox modulator. The cytoplasmic superoxide stress protein SodB was induced by acid, possibly in response to increased iron solubility. High pH induced amino acid metabolic enzymes (TnaA and CysK) as well as lac fusions to the genes encoding AstD and GabT. These enzymes participate in arginine and glutamate catabolic pathways that channel carbon into acids instead of producing alkaline amines. Overall, these data are consistent with a model in which E. coli modulates multiple transporters and pathways of amino acid consumption so as to minimize the shift of its external pH toward either acidic or alkaline extreme.

This article has been cited by other articles:

• Stewart, V. (2008). The Ribosome: a Metabolite-Responsive Transcription Regulator. J. Bacteriol. 190: 4787-4790 [Full Text]  
• Li, G., Ewers, C., Laturnus, C., Diehl, I., Alt, K., Dai, J., Antao, E.-M., Schnetz, K., Wieler, L. H. (2008). Characterization of a yjjQ mutant of avian pathogenic Escherichia coli (APEC). Microbiology 154: 1082-1093 [Abstract] [Full Text]  
• Wolfe, A. J., Parikh, N., Lima, B. P., Zemaitaitis, B. (2008). Signal Integration by the Two-Component Signal Transduction Response Regulator CpxR. J. Bacteriol. 190: 2314-2322 [Abstract] [Full Text]  
• Padalon-Brauch, G., Hershberg, R., Elgrably-Weiss, M., Baruch, K., Rosenshine, I., Margalit, H., Altuvia, S. (2008). Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36: 1913-1927 [Abstract] [Full Text]  
• Hernandez-Lucas, I., Gallego-Hernandez, A. L., Encarnacion, S., Fernandez-Mora, M., Martinez-Batallar, A. G., Salgado, H., Oropeza, R., Calva, E. (2008). The LysR-Type Transcriptional Regulator LeuO Controls Expression of Several Genes in Salmonella enterica Serovar Typhi. J. Bacteriol. 190: 1658-1670 [Abstract] [Full Text]  
• Abram, F., Su, W.-L., Wiedmann, M., Boor, K. J., Coote, P., Botting, C., Karatzas, K. A. G., O'Byrne, C. P. (2008). Proteomic Analyses of a Listeria monocytogenes Mutant Lacking {sigma}B Identify New Components of the {sigma}B Regulon and Highlight a Role for {sigma}B in the Utilization of Glycerol. Appl. Environ. Microbiol. 74: 594-604 [Abstract] [Full Text]  
• Golding, G. R., Sparling, R., Kelly, C. A. (2008). Effect of pH on Intracellular Accumulation of Trace Concentrations of Hg(II) in Escherichia coli under Anaerobic Conditions, as Measured Using a mer-lux Bioreporter. Appl. Environ. Microbiol. 74: 667-675 [Abstract] [Full Text]  
• Stolyar, S., He, Q., Joachimiak, M. P., He, Z., Yang, Z. K., Borglin, S. E., Joyner, D. C., Huang, K., Alm, E., Hazen, T. C., Zhou, J., Wall, J. D., Arkin, A. P., Stahl, D. A. (2007). Response of Desulfovibrio vulgaris to Alkaline Stress. J. Bacteriol. 189: 8944-8952 [Abstract] [Full Text]  
• Dupont, M., James, C. E., Chevalier, J., Pages, J.-M. (2007). An Early Response to Environmental Stress Involves Regulation of OmpX and OmpF, Two Enterobacterial Outer Membrane Pore-Forming Proteins. Antimicrob. Agents Chemother. 51: 3190-3198 [Abstract] [Full Text]  
• Wilks, J. C., Slonczewski, J. L. (2007). pH of the Cytoplasm and Periplasm of Escherichia coli: Rapid Measurement by Green Fluorescent Protein Fluorimetry. J. Bacteriol. 189: 5601-5607 [Abstract] [Full Text]  
• Zhang, X.-S., Garcia-Contreras, R., Wood, T. K. (2007). YcfR (BhsA) Influences Escherichia coli Biofilm Formation through Stress Response and Surface Hydrophobicity. J. Bacteriol. 189: 3051-3062 [Abstract] [Full Text]  
• Wei, Y., Deikus, G., Powers, B., Shelden, V., Krulwich, T. A., Bechhofer, D. H. (2006). Adaptive Gene Expression in Bacillus subtilis Strains Deleted for tetL.. J. Bacteriol. 188: 7090-7100 [Abstract] [Full Text]  
• Weber, A., Kogl, S. A., Jung, K. (2006). Time-Dependent Proteome Alterations under Osmotic Stress during Aerobic and Anaerobic Growth in Escherichia coli.. J. Bacteriol. 188: 7165-7175 [Abstract] [Full Text]  
• Roos, V., Klemm, P. (2006). Global Gene Expression Profiling of the Asymptomatic Bacteriuria Escherichia coli Strain 83972 in the Human Urinary Tract.. Infect. Immun. 74: 3565-3575 [Abstract] [Full Text]  
• Han, M.-J., Lee, S. Y. (2006). The Escherichia coli Proteome: Past, Present, and Future Prospects. Microbiol. Mol. Biol. Rev. 70: 362-439 [Abstract] [Full Text]  
• Trotochaud, A. E., Wassarman, K. M. (2006). 6S RNA Regulation of pspF Transcription Leads to Altered Cell Survival at High pH. J. Bacteriol. 188: 3936-3943 [Abstract] [Full Text]  
• Sturm, A., Schierhorn, A., Lindenstrauss, U., Lilie, H., Bruser, T. (2006). YcdB from Escherichia coli Reveals a Novel Class of Tat-dependently Translocated Hemoproteins. J. Biol. Chem. 281: 13972-13978 [Abstract] [Full Text]  
• Allen, M. J., White, G. F., Morby, A. P. (2006). The response of Escherichia coli to exposure to the biocide polyhexamethylene biguanide.. Microbiology 152: 989-1000 [Abstract] [Full Text]  
• Leaphart, A. B., Thompson, D. K., Huang, K., Alm, E., Wan, X.-F., Arkin, A., Brown, S. D., Wu, L., Yan, T., Liu, X., Wickham, G. S., Zhou, J. (2006). Transcriptome Profiling of Shewanella oneidensis Gene Expression following Exposure to Acidic and Alkaline pH. J. Bacteriol. 188: 1633-1642 [Abstract] [Full Text]  
• Pieterse, B., Leer, R. J., Schuren, F. H. J., van der Werf, M. J. (2005). Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151: 3881-3894 [Abstract] [Full Text]  
• Masse, E., Vanderpool, C. K., Gottesman, S. (2005). Effect of RyhB Small RNA on Global Iron Use in Escherichia coli. J. Bacteriol. 187: 6962-6971 [Abstract] [Full Text]  
• Marquart, M. E., Caballero, A. R., Chomnawang, M., Thibodeaux, B. A., Twining, S. S., O'Callaghan, R. J. (2005). Identification of a Novel Secreted Protease from Pseudomonas aeruginosa that Causes Corneal Erosions. IOVS 46: 3761-3768 [Abstract] [Full Text]  
• He, Z., Wu, L., Fields, M. W., Zhou, J. (2005). Use of Microarrays with Different Probe Sizes for Monitoring Gene Expression. Appl. Environ. Microbiol. 71: 5154-5162 [Abstract] [Full Text]  
• Hicks, W. M., Kotlajich, M. V., Visick, J. E. (2005). Recovery from long-term stationary phase and stress survival in Escherichia coli require the L-isoaspartyl protein carboxyl methyltransferase at alkaline pH. Microbiology 151: 2151-2158 [Abstract] [Full Text]  
• Handa, N., Terada, T., Doi-Katayama, Y., Hirota, H., Tame, J. R.H., Park, S.-Y., Kuramitsu, S., Shirouzu, M., Yokoyama, S. (2005). Crystal structure of a novel polyisoprenoid-binding protein from Thermus thermophilus HB8. Protein Sci. 14: 1004-1010 [Abstract] [Full Text]  
• Wolfe, A. J. (2005). The Acetate Switch. Microbiol. Mol. Biol. Rev. 69: 12-50 [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]  
• Joloba, M. L., Clemmer, K. M., Sledjeski, D. D., Rather, P. N. (2004). Activation of the gab Operon in an RpoS-Dependent Manner by Mutations That Truncate the Inner Core of Lipopolysaccharide in Escherichia coli. J. Bacteriol. 186: 8542-8546 [Abstract] [Full Text]  
• Sampathkumar, B., Khachatourians, G. G., Korber, D. R. (2004). Treatment of Salmonella enterica Serovar Enteritidis with a Sublethal Concentration of Trisodium Phosphate or Alkaline pH Induces Thermotolerance. Appl. Environ. Microbiol. 70: 4613-4620 [Abstract] [Full Text]  
• Ventura, M., Canchaya, C., van Sinderen, D., Fitzgerald, G. F., Zink, R. (2004). Bifidobacterium lactis DSM 10140: Identification of the atp (atpBEFHAGDC) Operon and Analysis of Its Genetic Structure, Characteristics, and Phylogeny. Appl. Environ. Microbiol. 70: 3110-3121 [Abstract] [Full Text]  
• Munson, R. S. Jr., Harrison, A., Gillaspy, A., Ray, W. C., Carson, M., Armbruster, D., Gipson, J., Gipson, M., Johnson, L., Lewis, L., Dyer, D. W., Bakaletz, L. O. (2004). Partial Analysis of the Genomes of Two Nontypeable Haemophilus influenzae Otitis Media Isolates. Infect. Immun. 72: 3002-3010 [Abstract] [Full Text]  
• Wen, Z. T., Burne, R. A. (2004). LuxS-Mediated Signaling in Streptococcus mutans Is Involved in Regulation of Acid and Oxidative Stress Tolerance and Biofilm Formation. J. Bacteriol. 186: 2682-2691 [Abstract] [Full Text]  
• Sharma, M., Beuchat, L. R. (2004). Sensitivity of Escherichia coli O157:H7 to Commercially Available Alkaline Cleaners and Subsequent Resistance to Heat and Sanitizers. Appl. Environ. Microbiol. 70: 1795-1803 [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]  
• Otto, K., Hermansson, M. (2004). Inactivation of ompX Causes Increased Interactions of Type 1 Fimbriated Escherichia coli with Abiotic Surfaces. J. Bacteriol. 186: 226-234 [Abstract] [Full Text]  
• Seputiene, V., Motiejunas, D., Suziedelis, K., Tomenius, H., Normark, S., Melefors, O., Suziedeliene, E. (2003). Molecular Characterization of the Acid-Inducible asr Gene of Escherichia coli and Its Role in Acid Stress Response. J. Bacteriol. 185: 2475-2484 [Abstract] [Full Text]  
• Schneider, B. L., Ruback, S., Kiupakis, A. K., Kasbarian, H., Pybus, C., Reitzer, L. (2002). The Escherichia coli gabDTPC Operon: Specific {gamma}-Aminobutyrate Catabolism and Nonspecific Induction. J. Bacteriol. 184: 6976-6986 [Abstract] [Full Text]