Metabolic regulation of Escherichia coli cultivated under anaerobic and aerobic conditions in response to the specific pathway gene knockouts

Abstract

Effect of the specific gene knockout on the main metabolism in Escherichia coli was reviewed, and the regulation mechanisms were clarified based on different levels of information such as gene expressions, enzyme activities, intracellular metabolite concentrations, and metabolic fluxes together with fermentation data. The effects of the knockout of such genes as pflA, pta, ppc, pykF, adhE, and ldhA on the metabolic changes were analyzed for the case under anaerobic condition. The effects of the knockout of such genes as pgi, zwf, gnd, ppc pck, pyk, and lpdA on the metabolic changes were also analyzed for the case under aerobic condition. The metabolic regulation analysis was made focusing on the roles of transcription factors.

Share and Cite:

Matsuoka, Y. and Shimizu, K. (2013) Metabolic regulation of Escherichia coli cultivated under anaerobic and aerobic conditions in response to the specific pathway gene knockouts. Advances in Bioscience and Biotechnology, 4, 455-468. doi: 10.4236/abb.2013.43A061.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Blattner, F.R., Plunkett 3rd, G., Bloch, C.A., Perna, N.T. Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., Gregor, J., Davis, N.W., Kirkpatrick, H.A., Goeden, M.A., Rose, D.J., Mau, B. and Shao, Y. (1997) The complete genome sequence of Escherichia coli K-12. Science, 277, 1453-1462. doi:10.1126/science.277.5331.1453
[2] Ohnishi, M., Tanaka, C., Kuhara, S., Ishii, K., Hattori, M., Kurokawa, K., Yasunaga, T., Makino, K., Shinagawa, H., Murata, T., Nakayama, K., Terawaki, Y. and Hayashi, T. (1999) Chromosome of the enterohemorrhagic Escherichia coli O157:H7; comparative analysis with K-12 MG 1655 revealed the acquisition of a large amount of foreign DNAs. DNA Research, 6, 361-368. doi:10.1093/dnares/6.6.361
[3] Steed, H., Macfarlane, G.T. and Macfarlane, S. (2008) Prebiotics, synbiotics and inflammatory bowel disease. Molecular Nutrtion and Food Research, 52, 898-905. doi:10.1002/mnfr.200700139
[4] Madan Babu, M. and Teichmann, S.A. (2003) Evolution of transcription factors and the gene regulatory network in Escherichia coli. Nucleic Acids Research, 31, 1234-1244. doi:10.1093/nar/gkg210
[5] Pérez-Rueda, E. and Collado-Vides, J. (2000) The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Research, 28, 1838-1847. doi:10.1093/nar/28.8.1838
[6] Gama-Costello, S., Salgado, H., Peralta-Gil, M., SantosZavaleta, A., Muniz-Rascado, L., Solano-Lira, H., JimenezJacinto, V., Weiss, V., Garcia-Sotelo, J.S., Lopez-Fuentes, A., Porron-Sotelo, L., Alquicira-Hernandez, S., MedinaRivera, A., Martinez-Flores, I., Alquicira-Hernandez, K., Martinez-Adame, R., Bonavides-Martinez, C., MirandaRios, J., Huerta, A.M., Mendoza-Vargas, A., ColladoTorres, L., Taboada, B., Vega-Alvarado, L., Olvera, M., Olvera, L., Grande, R., Morett, E. and Collado-Vides, J. (2011) RegulonDB version 7.0: Transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units). Nucleic Acids Research, 39, D98-105. doi:10.1093/nar/gkq1110
[7] Keseler I.M., Collado-Vides J., Santos-Zavaleta A., PeraltaGil, M., Gama-Castro, S., Muniz-Rascado, L., BonavidesMartinez, C., Paley, S., Krummenacker, M., Altman, T., Kaipa, P., Spaulding, A., Pacheco, J., Latendresse, M., Fulcher, C., Sarker, M., Shearer, A.G., Mackie, A., Paulsen, I., Gunsalus, R.P. and Karp, P.D. (2011) EcoCyc: A comprehensive database of Escherichia coli biology. Nucleic Acids Research, 39, D583-D590. doi:10.1093/nar/gkq1143
[8] Martínez-Antonio, A. (2011) Escherichia coli transcriptional regulatory network. Network Biology, 1, 21-33.
[9] Shimizu, K. (2012) Bacterial cellular metabolic systems. Woodhead Publishing Ltd., Cambridge.
[10] Shimizu, K. (2013) Metabolic regulation of a bacterial cell system with emphasis on Escherichia coli metabolism. International Scholarly Research Network Biochemistry, in Press.
[11] Kang, Y., Weber, K.D., Qiu, Y., Kiley, P.J. and Blattner, F.R. (2005) Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. Journal of Bacteriology, 187, 1135-1160. doi:10.1128/JB.187.3.1135-1160.2005
[12] Gunsalus, R.P. (1992) Control of electron flow in Escherichia coli: Coordinated transcription of respiratory pathway genes. Journal of Bacteriology, 174, 7069-7074.
[13] Alexeeva, S., Hellingwerf, K.J. and Teixeira de Mattos, M.J. (2003) Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. Journal of Bacteriology, 185, 204-209. doi:10.1128/JB.185.1.204-209.2003
[14] Zhu, J., Shalel-Levanon, S., Bennett, G. and San, K.Y. (2006) Effect of the global redox sensing/regulation networks on Escherichia coli and metabolic flux distribution based on C-13 labeling experiments. Metabolic Engineering, 8, 619-627. doi:10.1016/j.ymben.2006.07.002
[15] Levanon, S.S., San, K.Y. and Bennett, G.N. (2005) Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses. Biotechnology and Bioengineering, 89, 556-564. doi:10.1002/bit.20381
[16] Shalel-Levanon, S., San, K.Y. and Bennett, G.N. (2005) Effect of oxygen, and ArcA and FNR regulators on the expression of genes related to the electron transfer chain and the TCA cycle in Escherichia coli. Metabolic Engineering, 7, 364-374. doi:10.1016/j.ymben.2005.07.001
[17] Zhu, J. and Shimizu, K. (2004) The effect of pfl genes knockout on the metabolism for optically pure D-lactate production by Escherichia coli. Applied Microbiology and Biotechnology, 64, 367-375. doi:10.1007/s00253-003-1499-9
[18] Zhu, J. and Shimizu, K. (2005) Effect of a single-gene knockout on the metabolic regulation in E. coli for Dlactate production under microaerobic condition. Metabolic Engineering, 7, 104-115. doi:10.1016/j.ymben.2004.10.004
[19] Alexeeva, S., de Kort, B., Sawers, G., Hellingwerf, K.J. and de Mattos, M.J. (2000) Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli. Journal of Bacteriology, 182, 4934-4940. doi:10.1128/JB.182.17.4934-4940.2000
[20] Vemuri, G.N., Minning, T.A., Altman, E. and Eiteman, M.A. (2005) Physiological response of central metabolism in Escherichia coli to deletion of pyruvate oxidase and introduction of heterologous pyruvate carboxylase. Biotechnology and Bioengineering, 90, 64-76. doi:10.1002/bit.20418
[21] Georgellis, D., Kwon, O. and Lin, E.C. (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science, 292, 2314-2316. doi:10.1126/science.1059361
[22] Malpica, R., Franco, B., Rodriquez, C., Kwon, O. and Georgellis, D. (2004) Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proceedings of the National Academy of Sciences of the United States of America, 101, 13318-13323. doi:10.1073/pnas.0403064101
[23] Nizam, S.A., Zhu, J.F., Ho, P.Y. and Shimizu, K. (2009) Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under aerobic condition. Biochemical Engineering Journal, 44, 240-250. doi:10.1016/j.bej.2008.12.017
[24] Vemuri, G.N., Altman, E., Sangurdekar, D.P., Khodursky, A.B. and Eiteman, M.A. (2006) Overflow metabolism in Escherichia coli during steady-state growth: Transcriptional regulation and effect of the redox ratio. Applied and Environmental Microbiology, 72, 3653-3661. doi:10.1128/AEM.72.5.3653-3661.2006
[25] Vemuri, G.N., Eiteman, M.A. and Altman, E. (2006) Increased recombinant protein production in Escherichia coli strains with overexpressed water-forming NADH oxidase and a deleted ArcA regulatory protein. Biotechnology and Bioengineering, 94, 538-542. doi:10.1002/bit.20853
[26] Nizam, S.A. and Shimizu, K. (2008) Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under anaerobic and microaerobic conditions. Biochemical Engineering Journal, 42, 229-236. doi:10.1016/j.bej.2008.06.021
[27] Crack, J.C., Le Brun, N.E., Thomson, A.J., Green, J. and Jervis, A.J. (2008) Reactions of nitric oxide and oxygen with the regulator of fumarate and nitrate reduction, a global transcriptional regulator, during anaerobic growth of Escherichia coli. Methods in Enzymology, 437, 191-209. doi:10.1016/S0076-6879(07)37011-0
[28] Green, J. and Guest, J.R. (1993) Activation of FNR-dependent transcription by iron: An in vitro switch for FNR. FEMS Microbiology Letters, 113, 219-222. doi:10.1111/j.1574-6968.1993.tb06517.x
[29] Kiley, P.J. and Reznikoff, W.S. (1991) Fnr mutants that activate gene expression in the presence of oxygen. Journal of Bacteriology, 173, 16-22.
[30] Marzan, L.W., Siddiquee, K.A. and Shimizu, K. (2011) Metabolic regulation of an fnr gene knockout Escherichia coli under oxygen limitation. Bioengineered Bugs, 2, 331-337. doi:10.4161/bbug.2.6.16350
[31] Toya, Y., Nakahigashi, K., Tomita, M. and Shimizu, K. (2012) Metabolic regulation analysis of wild-type and arcA mutant Escherichia coli under nitrate conditions using different levels of omics data. Molecular BioSystems, 8, 2593-2604. doi:10.1039/c2mb25069a
[32] Sauer, U. (2006) Metabolic networks in motion: 13Cbased flux analysis. Molecular Systems Biology, 2, 62. doi:10.1038/msb4100109
[33] Garrigues, C. Loubiere, P., Lindley, N.D. and CocaignBousquet, M. (1997) Control of the shift from homolactic acids to mixed-acid fermentation in Lactococcus lactis: Predominant role of the NADH/NAD+ ratio. Journal of Bacteriology, 179, 5282-5287.
[34] De Graef, M.R., Alexeeva, S., Snoep, J.L. and Teixeira de Mattos, M.J. (1999) The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. Journal of Bacteriology, 181, 2351-2357.
[35] Smith, T.E., Balasubramanian, K.A. and Beezley, A. (1980) Escherichia coli phosphoenolpyruvate carboxylase. Studies on the mechanism of synergistic activation by nucleotides. The Journal of Biological Chemistry, 255, 1635-1642.
[36] McAlister, L.E., Evans, E.L. and Smith, T.E. (1981) Properties of a mutant Escherichia coli phosphoenolpyruvate carboxylase deficient in coregulation by intermediary metabolites. Journal of Bacteriology, 146, 200-208.
[37] Koebmann, B.J., Westerhoff, H.V., Snoep, J.L., Nilsson, D. and Jensen, P.R. (2002) The glycolytic flux in Escherichia coli is controlled by the demand for ATP. Journal of Bacteriology, 184, 3909-3916. doi:10.1128/JB.184.14.3909-3916.2002
[38] Kabir, M.M., Ho, P.Y. and Shimizu, K. (2005) Effect of ldhA gene deletion on the metabolism of Escherichia coli based on gene expression, enzyme activities intracellular metabolite concentrations, and metabolic flux distribution. Biochemical Engineering Journal, 26, 1-11. doi:10.1016/j.bej.2005.05.010
[39] Yao, R., Hirose, Y., Sarkar, D., Nakahigashi, K., Ye, Q. and Shimizu, K. (2011) Catabolic regulation analysis of Escherichia coli and its crp, mlc, mgsA, pgi and ptsG mutants. Microbial Cell Factories, 10, 67. doi:10.1186/1475-2859-10-67
[40] Bettenbrock, K., Fischer, S., Klemling, A., Sauter, F.T. and Gilles, E.D. (2006) A quantitative approach to catabolite repression in Escherichia coli. The Journal of Biological Chemistry, 281, 2578-2584. doi:10.1074/jbc.M508090200
[41] Gorke, B. and Stulke, J. (2008) Carbon catabolite repression in bacteria: Many ways to make the most out of nutrients. Nature Reviews Microbiology, 6, 613-624. doi:10.1038/nrmicro1932
[42] Park, Y.H., Lee, B.R., Seok, Y.J. and Peterkofsky, A. (2006) In vitro reconstruction of catabolite repression in Escherichia coli. The Journal of Biological Chemistry, 281, 6448-6454. doi:10.1074/jbc.M512672200
[43] Bettenbrock, K., Sauter, T., Jahreis, K., Klemling, A., Lengeler, J.W. and Gilles, E.D. (2007) Correlation between growth rates, EIIACrr phosphorylation, and intracellular cyclic AMP levels in Escherichia coli K-12. Journal of Bacteriology, 189, 6891-6900. doi:10.1128/JB.00819-07
[44] Hogema, B.M., Arents, J.C., Bader, R., Eijkemans, K., Yoshida, H., Takahashi, H., Aiba, H. and Postma, P.W. (1998) Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mo-lecular Microbiology, 30, 487-498. doi:10.1046/j.1365-2958.1998.01053.x
[45] Moat, A.G., Foster, J.W. and Spector, M.P. (2002) Microbial physiology. 4th Edition, Wiley-Liss Inc., New York. doi:10.1002/0471223867
[46] Saier Jr., M.H., Ramseier, T.M. and Reizer, J. (1996) Regulation of carbon utilization. In: Neidhardt, F.C., Curtiss III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M. and Umbarger, H.E. Ed., Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd Edition, ASM Press, Washington DC, 1325-1343.
[47] Saier Jr., M.H. and Ramseier, T.M. (1996) The catabolite repressor/activator (Cra) protein of enteric bacteria. Journal of Bacteriology, 178, 3411-3417.
[48] Sarkar, D. and Shimizu, K. (2008) Effect of cra gene knockout together with other genes knockouts on the improvement of substrate consumption rate in Escherichia coli under microaerobic conditions. Biochemical Engineering Journal, 42, 224-228. doi:10.1016/j.bej.2008.06.019
[49] Canonaco, F., Hess, T.A., Heri, S., Wang, T., Szyperski, T. and Sauer, U. (2001) Metabolic flux response to phosphoglucose isomerase knock-out in Escherichia coli and impact of overexpression of the soluble transhydrogenase UdhA. FEMS Microbiology Letters, 204, 247-252. doi:10.1111/j.1574-6968.2001.tb10892.x
[50] Fischer, E. and Sauer, U. (2003) Metabolic flux profiling of Escherichia coli mutants in central carbon metabolism using GC-MS. European Journal of Biochemistry, 270, 880-891. doi:10.1046/j.1432-1033.2003.03448.x
[51] Hua, Q., Yang, C., Baba, T., Mori, H. and Shimizu, K. (2003) Responses of the central carbon metabolism in Escherichia coli to phosphoglucose isomerase and glucose6-phosphate dehydrogenase knockouts. Journal of Bacteriology, 185, 7053-7067. doi:10.1128/JB.185.24.7053-7067.2003
[52] Toya, Y., Ishii, N., Nakahigashi, K., Hirasawa, T., Soga, T., Tomita, M. and Shimizu, K. (2010)13C-metabolic flux analysis for batch culture of Escherichia coli and its pyk and pgi gene knockout mutants based on mass isotopomer distribution of intracellular metabolites. Biotechnology Progress, 26, 975-992. doi:10.1002/btpr.420
[53] Yang, C., Hua, Q., Baba, T., Mori, H. and Shimizu, K. (2003) Analysis of Escherichia coli anaprelotic metabolism and its regulation mechanisms from the metabolic responses to altered dilution rates and phosphoenolpyruvate carboxykinase knockout. Biotechnology and Bioengineering, 84, 129-144. doi:10.1002/bit.10692
[54] Zhao, J., Baba, T., Mori, H. and Shimizu, K. (2004) Effect of zwf gene knockout on the metabolism of Escherichia coli grown on glucose or acetate. Metabolic Engineering, 6, 164-174. doi:10.1016/j.ymben.2004.02.004
[55] Jiao, Z., Baba, T., Mori, H. and Shimizu, K. (2003) Analysis of metabolic and physiological responses to gnd knockout in E. coli by using C-13 tracer experiment and enzyme activity measurement. FEMS Microbiology Letters, 220, 295-301. doi:10.1016/S0378-1097(03)00133-2
[56] Choi, I.Y., Sup, K.I., Kim, H.J. and Park, J.W. (2003) Thermosensitive phenotype of Escherichia colimutant lacking NADP+-dependent isocitrate dehydrogenase. Redox Report, 8, 51-56. doi:10.1179/135100003125001251
[57] Farmer, W.R. and Liao, J.C. (1997) Reduction of aerobic acetate production by Escherichia coli. Applied and Environmental Microbiology, 63, 3205-3210.
[58] Peng, L. and 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 and Microbial Technology, 38, 512-520. doi:10.1016/j.enzmictec.2005.07.019
[59] Peng, L., Arauzo, M. and Shimizu, K. (2004) Metabolic flux analysis for a ppc mutant Escherichia coli based on 13C-labelling experiments together with enzyme activity assays and intracellular metabolite measurements. FEMS Microbiology Letters, 235, 17-23. doi:10.1111/j.1574-6968.2004.tb09562.x
[60] Fraenkel, D.G. and Neidhardt, F. (eds) (1999) Escherichia coli and Salmonella: Cellular and molecular biology. American Society for Microbiology Press, Washington DC.
[61] Sugimoto, S. and Shiio, I. (1987) Regulation of 6-phosphogluconate dehydrogenase in Brevibacterium flavum. Agriculture and Biological Chemistry, 51, 1257-1263. doi:10.1271/bbb1961.51.1257
[62] Morita, T., EI-Kazzaz, W., Tanaka, Y., Inada, T. and Aiba, H. (2003) Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli. The Journal of Biological Chemistry, 278, 15608-15614. doi:10.1074/jbc.M300177200
[63] Krebs, A. and Bridger, W.A. (1980) The kinetic properties of phosphoenolpyruvate carboxykinase of Escherichia coli. Canadian Journal of Biochemistry, 58, 309-318. doi:10.1139/o80-041
[64] Al Zaid Siddiquee, K., Arauzo-Bravo, M.J. and Shimizu, K. (2004) Metabolic flux analysis of pykF gene knockout Escherichia coli based on 13C-labeled experiment together with measurements of enzyme activities and intracellular metabolite concentrations. Applied Microbiology and Biotechnology, 63, 407-417. doi:10.1007/s00253-003-1357-9
[65] Siddiquee, K.A.Z., Arauzo-Bravo, M. and Shimizu, K. (2004) Effect of pyruvate kinase (pykF gene) knockout mutation on the control of gene expression and metabolic fluxes in Escherichia coli. FEMS Microbiology Letters, 235, 25-33. doi:10.1016/j.femsle.2004.04.004
[66] Kedar, P., Colah, R. and Shimizu, K. (2007) Proteomic investigation on the pyk-F gene knockout Escherichia coli for aromatic amino acid production. Enzyme and Microbial Technology, 41, 455-465. doi:10.1016/j.enzmictec.2007.03.018
[67] Li, M., Yao, S. and 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. Journal of Biotechnology, 122, 254-266. doi:10.1016/j.jbiotec.2005.09.016
[68] Li, M., Ho, P.Y., Yao, S. and Shimizu, K. (2006) Effect of sucA or sucC gene knockout on the metabolism in Escherichia coli based on gene expressions, enzyme activeties, intracellular metabolite concentrations and metabolic fluxes by 13C-labeling experiments. Biochemical Engineering Journal, 30, 286-296. doi:10.1016/j.bej.2006.05.011
[69] Abdel-Hamid, A.M., Attwood, M.M. and Guest, J.R. (2001) Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia coli. Microbiology, 147, 1483-1498.
[70] Dietrich, J. and Henning, U. (1970) Regulation of pyruvate dehydrogenase complex synthesis in Escherichia coli K 12. Identification of the inducing metabolite. European Journal of Biochemistry, 14, 258-269. doi:10.1111/j.1432-1033.1970.tb00285.x

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.