Abstract
Metabolic regulation in Escherichia coli was studied in terms of the changes in the expression of the global regulatory genes rpoD, rpoS, soxRS, cra, fadR, iclR and arcA at three different growth phases, in batch culture. The expression of rpoS and several rpoS-dependent metabolic pathway genes, such as tktB, talA, fumC, acnA, sucA, acs and sodC, were increased (∼1.5 to 2-fold) as the cells entered the late phase of growth. The changes in the expression of other global regulators and their effects on different metabolic pathway genes were less significant, as compared to rpoS, during the later phases of growth.
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Alexeeva S, Hellingwerf KJ, Joost Teixeira de Mattos M (2003) Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. J Bacteriol 185:204–209
Aronis HR (2002a) Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Microbiol Rev 66:373–395
Aronis HR (2002b) Stationary phase gene regulation: what makes an Escherichia coli promoter sigmaS-selective? Curr Opin Microbiol 5:591–595
Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008
Bergmeyer HU (1984) Methods of enzymatic analysis, 3rd edn, vol VI. VCH, Weinheim
Bergmeyer HU (1985) Methods of enzymatic analysis, 3rd edn, vol VII. VCH, Weinheim
Bledig SA, Ramseier TM, Saier MH Jr (1996) FruR mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J Bacteriol 178:280–283
Chen DP, Tseng CP, Lin HT, Sun CF (2001) Oxygen- and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity. J Bacteriol 183:461–467
Cortay JC, Negre D, Galinier A, Duclos B, Perriere G, Cozzone AJ (1991) Regulation of the acetate operon in Escherichia coli: purification and functional characterization of the IclR repressor. EMBO 10:675–679
Cronan JE, LaPorte DJ (1996) Tricarboxylic acid cycle and glyoxylate bypass. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM Press, Washington, DC, pp 208–211
El-Mansi EMT, MacKintosh C, Duncan K, Holms WH, Nimmo HG (1987) Molecular cloning and over-expression of the glyoxylate bypass operon from Escherichia coli ML308. Biochem J 242:661–665
Gui L, Sunnarborg A, LaPorte DC (1996) Regulated expression of a repressor protein: FadR activates iclR. J Bacteriol 178:4704–4709
Jishage M, Iwata A, Ueda S, Ishihama A (1996) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol 178:5447–5451
Jordan PA, Tang Y, Bradbury AJ, Thomson AJ, Guest JR (1999) Biochemical and spectroscopic characterization of Escherichia coli aconitases (AcnA and AcnB). Biochem J 344:739–746
Kabir MM, Shimizu K (2003) Gene Expression patterns for metabolic pathway in pgi knockout Escherichia coli with and without phb genes based on RT-PCR. J Biotechnol 105:11–31
Krapp AR, Rodriguez RE, Poli HO, Paladini DH, Palatnik JF, Carrillo N (2002) The flavoenzyme ferredoxin (flavodoxin)-NADP(H) reductase modulates NADP(H) homeostasis during the soxRS response of Escherichia coli. J Bacteriol 184:1474–1480
Kumari S, Beatty CM, Browning DF, Busby SJW, Simel EJ, Hovel-Miner G, Wolfe AJ (2000) Regulation of acetyl coenzyme a synthetase in Escherichia coli. J Bacteriol 182:4173–4179
Lacour S, Landini P (2004) SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σS-dependent genes and identification of their promoter sequences. J Bacteriol 186:7186–7195
Levanon S, San KY, Bennett GN (2005) Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses. Biotechnol Bioeng 89:556–564
Li M, Ho PY, Yao S, Shimizu K (2006) Effect of lpdA gene knockout on the metabolism in Escherichia coli based on enzyme activities, intracellular metabolite concentrations and metabolic flux analysis by 13C-labeling experiments. J Biotechnol 122:254–266
Lin H, Castro NM, Bennett GN, San KY (2006) Acetyl-CoA synthetase overexpression in Escherichia coli demonstrates more efficient acetate assimilation and lower acetate accumulation: a potential tool in metabolic engineering. Appl Microbiol Biotechnol 71:870–874
Liochev SI, Fridovich I (1992) Fumarase C, the stable fumarase of Escherichia coli, is controlled by the soxRS regulon. Proc Natl Acad Sci USA 89:5892–5896
Lu C, Bentley WE, Rao G (2003) Comparison of oxidative stress response genes in aerobic Escherichia coli fermentations. Biotechnol Bioeng 83:864–870
Moat AG, Foster JW, Spector MP (2002) Microbial physiology. John Wiley & Sons, Inc, Singapore
Park SJ, Gunsalus RP (1995) Oxygen, iron, carbon, and super-oxide control of the fumarase fumA and fumC genes of Escherichia coli: role of the arcA, fnr, and soxR gene products. J Bacteriol 177:6255–6262
Patten CL, Kirchhof MG, Schertzberg MR, Morton RA, Schellhorn HE (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Gen Genomics 272:580–591
Peng L, Shimizu K (2003) Global metabolic regulation analysis for Escherichia coli K-12 based on protein expression by 2D electrophoresis and enzyme activity measurement. Appl Microbiol Biotechnol 61:163–178
Peng L, Shimizu K (2006) Effect of fadR gene knockout on the metabolism of Escherichia coli based on analyses of protein expressions, enzyme activities and intracellular metabolite concentrations. Enzyme Microb Technol 38:512–520
Perrenoud A, Sauer U (2005) Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. J Bacteriol 187:3171–3179
Rahman M, Hasan MR, Oba T, Shimizu K (2006) Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expression, enzyme activities and intracellular metabolite concentrations. Biotechnol Bioeng 94:585–595
Siddiquee KAZ, Arauzo-Bravo MJ, Shumizu K (2004) Metabolic flux analysis of pykF gene knockout Escherichia coli based on 13C-labeling experiments together with measurements of enzyme activities and intracellular metabolite concentrations. Appl Microbiol Biotechnol 63:407–417
Stryer L (1988) Biochemistry. W. H. Freeman and Company, New York, pp 511–512
Tang Y, Quail MA, Artymiuk PJ, Guest JR, Green J (2002) Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression. Microbiol 148:1027–1037
Varghese S, Tang Y, Imlay JA (2003) Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J Bacteriol 185:221–230
Vijaykumar SRV, Kirchhof MG, Patten CL, Schellhorn HE (2004) RpoS-regulated genes of Escherichia coli identified by random lacZ fusion mutagenesis. J Bacteriol 186:8499–8507
Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603
Zhu J, Shimizu K (2004) The effect of pfl knockout on the metabolism for optically pure D-lactate production by Escherichia coli. Appl Microbiol Biotechnol 64:367–375
Acknowledgement
We would like to thank Prof. Mori of Keio University, Japan for providing us with the E. coli strain BW25113. Thanks are also due to Brie Fuqua of UC Berkeley, CA, USA for editing the manuscript.
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Rahman, M., Hasan, M.R. & Shimizu, K. Growth phase-dependent changes in the expression of global regulatory genes and associated metabolic pathways in Escherichia coli . Biotechnol Lett 30, 853–860 (2008). https://doi.org/10.1007/s10529-007-9621-1
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DOI: https://doi.org/10.1007/s10529-007-9621-1