This Article 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 Wanner, B L Articles by Wilmes-Riesenberg, M R Search for Related Content PubMed PubMed Citation Articles by Wanner, B L Articles by Wilmes-Riesenberg, M R

research-article

Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli.

Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907.

ABSTRACT

Two controls of the phosphate (PHO) regulon require sensor proteins that are protein kinases that phosphorylate the regulator, PhoB, which in turn activates transcription only when phosphorylated. Pi control requires the Pi sensor PhoR; the other control is Pi independent and requires the sensor CreC (formerly called PhoM). Here we describe an additional control of the PHO regulon which is Pi independent and requires neither PhoR nor CreC. This control is regulated by a two-step pathway in carbon metabolism in which acetyl coenzyme A, Pi, and ADP are converted into acetate, coenzyme A, and ATP via the enzymes phosphotransacetylase (Pta) and acetate kinase (AckA). It responds to the synthesis of acetyl phosphate, an intermediate in the Pta-AckA pathway. Since the synthesis of acetyl phosphate via this pathway leads to the incorporation of Pi into ATP, the primary phosphoryl donor in metabolism, we propose that a regulatory coupling(s) may exist between the PHO regulon, which encodes genes for Pi uptake, and genes for enzymes in central metabolism for incorporation of Pi into ATP. Regulatory interactions of this sort may be important in global control. Further, it provides a functional basis for the concept of cross-regulation in the PHO regulon. This is also the first evidence that acetyl phosphate may have a role as an effector of gene regulation.

This article has been cited by other articles:

• Cariss, S. J. L., Tayler, A. E., Avison, M. B. (2008). Defining the Growth Conditions and Promoter-Proximal DNA Sequences Required for Activation of Gene Expression by CreBC in Escherichia coli. J. Bacteriol. 190: 3930-3939 [Abstract] [Full Text]  
• Cabeza, M. L., Aguirre, A., Soncini, F. C., Vescovi, E. G. (2007). Induction of RpoS Degradation by the Two-Component System Regulator RstA in Salmonella enterica. J. Bacteriol. 189: 7335-7342 [Abstract] [Full Text]  
• Glover, R. T., Kriakov, J., Garforth, S. J., Baughn, A. D., Jacobs, W. R. Jr. (2007). The Two-Component Regulatory System senX3-regX3 Regulates Phosphate-Dependent Gene Expression in Mycobacterium smegmatis. J. Bacteriol. 189: 5495-5503 [Abstract] [Full Text]  
• Klein, A. H., Shulla, A., Reimann, S. A., Keating, D. H., Wolfe, A. J. (2007). The Intracellular Concentration of Acetyl Phosphate in Escherichia coli Is Sufficient for Direct Phosphorylation of Two-Component Response Regulators. J. Bacteriol. 189: 5574-5581 [Abstract] [Full Text]  
• Jensen, V., Lons, D., Zaoui, C., Bredenbruch, F., Meissner, A., Dieterich, G., Munch, R., Haussler, S. (2006). RhlR Expression in Pseudomonas aeruginosa Is Modulated by the Pseudomonas Quinolone Signal via PhoB-Dependent and -Independent Pathways. J. Bacteriol. 188: 8601-8606 [Abstract] [Full Text]  
• Monds, R. D., Newell, P. D., Schwartzman, J. A., O'Toole, G. A. (2006). Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1.. Appl. Environ. Microbiol. 72: 1910-1924 [Abstract] [Full Text]  
• Lawrence, S. H., Luther, K. B., Schindelin, H., Ferry, J. G. (2006). Structural and Functional Studies Suggest a Catalytic Mechanism for the Phosphotransacetylase from Methanosarcina thermophila. J. Bacteriol. 188: 1143-1154 [Abstract] [Full Text]  
• Ghorbel, S., Kormanec, J., Artus, A., Virolle, M.-J. (2006). Transcriptional Studies and Regulatory Interactions between the phoR-phoP Operon and the phoU, mtpA, and ppk Genes of Streptomyces lividans TK24. J. Bacteriol. 188: 677-686 [Abstract] [Full Text]  
• Batchelor, E., Walthers, D., Kenney, L. J., Goulian, M. (2005). The Escherichia coli CpxA-CpxR Envelope Stress Response System Regulates Expression of the Porins OmpF and OmpC. J. Bacteriol. 187: 5723-5731 [Abstract] [Full Text]  
• Pena-Sandoval, G. R., Kwon, O., Georgellis, D. (2005). Requirement of the Receiver and Phosphotransfer Domains of ArcB for Efficient Dephosphorylation of Phosphorylated ArcA In Vivo. J. Bacteriol. 187: 3267-3272 [Abstract] [Full Text]  
• Wolfe, A. J. (2005). The Acetate Switch. Microbiol. Mol. Biol. Rev. 69: 12-50 [Abstract] [Full Text]  
• Runyen-Janecky, L. J., Boyle, A. M., Kizzee, A., Liefer, L., Payne, S. M. (2005). Role of the Pst System in Plaque Formation by the Intracellular Pathogen Shigella flexneri. Infect. Immun. 73: 1404-1410 [Abstract] [Full Text]  
• Joyce, E. A., Kawale, A., Censini, S., Kim, C. C., Covacci, A., Falkow, S. (2004). LuxS Is Required for Persistent Pneumococcal Carriage and Expression of Virulence and Biosynthesis Genes. Infect. Immun. 72: 2964-2975 [Abstract] [Full Text]  
• Kim, D.-j., Boylan, B., George, N., Forst, S. (2003). Inactivation of ompR Promotes Precocious Swarming and flhDC Expression in Xenorhabdus nematophila. J. Bacteriol. 185: 5290-5294 [Abstract] [Full Text]  
• Lesley, J. A., Waldburger, C. D. (2003). Repression of Escherichia coli PhoP-PhoQ Signaling by Acetate Reveals a Regulatory Role for Acetyl Coenzyme A. J. Bacteriol. 185: 2563-2570 [Abstract] [Full Text]  
• Carmany, D. O., Hollingsworth, K., McCleary, W. R. (2003). Genetic and Biochemical Studies of Phosphatase Activity of PhoR. J. Bacteriol. 185: 1112-1115 [Abstract] [Full Text]  
• Verhamme, D. T., Arents, J. C., Postma, P. W., Crielaard, W., Hellingwerf, K. J. (2002). Investigation of in vivo cross-talk between key two-component systems of Escherichia coli. Microbiology 148: 69-78 [Abstract] [Full Text]  
• Leighton, M. P., Kelly, D. J., Williamson, M. P., Shaw, J. G. (2001). An NMR and enzyme study of the carbon metabolism of Neisseria meningitidis. Microbiology 147: 1473-1482 [Abstract] [Full Text]  
• Hunt, M. L., Boucher, D. J., Boyce, J. D., Adler, B. (2001). In Vivo-Expressed Genes of Pasteurella multocida. Infect. Immun. 69: 3004-3012 [Abstract] [Full Text]  
• Buss, K. A., Cooper, D. R., Ingram-Smith, C., Ferry, J. G., Sanders, D. A., Hasson, M. S. (2001). Urkinase: Structure of Acetate Kinase, a Member of the ASKHA Superfamily of Phosphotransferases. J. Bacteriol. 183: 680-686 [Abstract] [Full Text]  
• Heyde, M., Laloi, P., Portalier, R. (2000). Involvement of Carbon Source and Acetyl Phosphate in the External-pH-Dependent Expression of Porin Genes in Escherichia coli. J. Bacteriol. 182: 198-202 [Abstract] [Full Text]  
• Nakano, M. M., Zhu, Y., Haga, K., Yoshikawa, H., Sonenshein, A. L., Zuber, P. (1999). A Mutation in the 3-Phosphoglycerate Kinase Gene Allows Anaerobic Growth of Bacillus subtilis in the Absence of ResE Kinase. J. Bacteriol. 181: 7087-7097 [Abstract] [Full Text]  
• Cunning, C., Elliott, T. (1999). RpoS Synthesis Is Growth Rate Regulated in Salmonella typhimurium, but Its Turnover Is Not Dependent on Acetyl Phosphate Synthesis or PTS Function. J. Bacteriol. 181: 4853-4862 [Abstract] [Full Text]  
• McDowall, K. J., Thamchaipenet, A., Hunter, I. S. (1999). Phosphate Control of Oxytetracycline Production by Streptomyces rimosus Is at the Level of Transcription from Promoters Overlapped by Tandem Repeats Similar to Those of the DNA-Binding Sites of the OmpR Family. J. Bacteriol. 181: 3025-3032 [Abstract] [Full Text]  
• Bock, A.-K., Glasemacher, J., Schmidt, R., Schönheit, P. (1999). Purification and Characterization of Two Extremely Thermostable Enzymes, Phosphate Acetyltransferase and Acetate Kinase, from the Hyperthermophilic Eubacterium Thermotoga maritima. J. Bacteriol. 181: 1861-1867 [Abstract] [Full Text]  
• Gibson, K. E., Silhavy, T. J. (1999). The LysR Homolog LrhA Promotes RpoS Degradation by Modulating Activity of the Response Regulator SprE. J. Bacteriol. 181: 563-571 [Abstract] [Full Text]  
• Silva, J. C., Haldimann, A., Prahalad, M. K., Walsh, C. T., Wanner, B. L. (1998). In vivo characterization of the type A and B vancomycin-resistant enterococci (VRE) VanRS two-component systems in Escherichia coli: A nonpathogenic model for studying the VRE signal transduction pathways. Proc. Natl. Acad. Sci. USA 95: 11951-11956 [Abstract] [Full Text]  
• Bardin, S. D., Finan, T. M. (1998). Regulation of Phosphate Assimilation in Rhizobium (Sinorhizobium) meliloti. Genetics 148: 1689-1700 [Abstract] [Full Text]  
• Singh-Wissmann, K., Ingram-Smith, C., Miles, R. D., Ferry, J. G. (1998). Identification of Essential Glutamates in the Acetate Kinase from Methanosarcina thermophila. J. Bacteriol. 180: 1129-1134 [Abstract] [Full Text]  
• Haldimann, A., Daniels, L. L., Wanner, B. L. (1998). Use of New Methods for Construction of Tightly Regulated Arabinose and Rhamnose Promoter Fusions in Studies of the Escherichia coli Phosphate Regulon. J. Bacteriol. 180: 1277-1286 [Abstract] [Full Text]  
• Haldimann, A., Prahalad, M. K., Fisher, S. L., Kim, S.-K., Walsh, C. T., Wanner, B. L. (1996). Altered recognition mutants of the response regulator PhoB: A new genetic strategy for studying protein-protein interactions. Proc. Natl. Acad. Sci. USA 93: 14361-14366 [Abstract] [Full Text]  
• Kehoe, D. M., Grossman, A. R. (1996). Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors. Science 273: 1409-1412 [Abstract]  
• Fisher, S. L., Jiang, W., Wanner, B. L., Walsh, C. T. (1995). Cross-talk between the Histidine Protein Kinase VanS and the Response Regulator PhoB. J. Biol. Chem. 270: 23143-23149 [Abstract] [Full Text]  
• Danese, P N, Snyder, W B, Cosma, C L, Davis, L J, Silhavy, T J (1995). The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP.. Genes Dev. 9: 387-398 [Abstract]  
• Avison, M. B., Horton, R. E., Walsh, T. R., Bennett, P. M. (2001). Escherichia coli CreBC Is a Global Regulator of Gene Expression That Responds to Growth in Minimal Media. J. Biol. Chem. 276: 26955-26961 [Abstract] [Full Text]