Catabolite regulation analysis of Escherichia coli for acetate overflow mechanism and co-consumption of multiple sugars based on systems biology approach using computer simulation

Journal of Biotechnology

Volumn 168, Issue 2, 2013, Pages 155-173

  Matsuoka, Yu ^a   Shimizu, Kazuyuki ^a,b  

^a KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^b KEIO UNIVERSITY   (Japan)

Author keywords

Catabolite regulation; Computer simulation; Escherichia coli; Modeling; Multiple carbon sources; Systems biology

Indexed keywords

CARBON SOURCE; CATABOLITE REGULATION; GLUCOSE CONSUMPTION RATE; METABOLIC CHARACTERISTICS; PERTURBATION ANALYSIS; PHOSPHOTRANSFERASE SYSTEM; REGULATION MECHANISMS; SYSTEMS BIOLOGY;

CARBON; ESCHERICHIA COLI; FERMENTATION; GLUCOSE; METABOLISM; MODELS; PATHOLOGY; PHYSIOLOGY; VOLATILE FATTY ACIDS;

COMPUTER SIMULATION;

ACETIC ACID; CARBOHYDRATE; CYCLIC AMP; GLUCOSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CRA; UNCLASSIFIED DRUG; XYLOSE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; CARBON SOURCE; CITRIC ACID CYCLE; COMPUTER SIMULATION; ESCHERICHIA COLI; FEEDBACK SYSTEM; FERMENTATION; GENE EXPRESSION; GLUCOSE INTAKE; GLUCOSE TRANSPORT; GLYCOLYSIS; KNOCKOUT GENE; METABOLIC REGULATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; WILD TYPE;

ESCHERICHIA COLI;

6-PHOSPHOGLUCONATE; 6-PHOSPHOGLUCONATE DEHYDROGENASE; 6PG; ACETATE KINASE; ACETYL COENZYME A SYNTHETASE; ACK; ACS; ADENYLATE CYCLASE; CARBON CATABOLITE REPRESSION; CATABOLITE REGULATION; CCR; CIT; CITRATE; CITRATE SYNTHASE; COMPUTER SIMULATION; CS; CYA; E4P; EI; EII; ENO; ENOLASE; ENZYME I; ENZYME II; ERYTHROSE-4-PHOSPHATE; ESCHERICHIA COLI; F6P; FBP; FDP; FRUCTOSE BISPHOSPHATASE; FRUCTOSE-1.6-BISPHOSPHATE; FRUCTOSE-6-PHOSPHATE; G6P; G6PDH; GAP; GF6P; GLC; GLK; GLUCOKINASE; GLUCOSE; GLUCOSE-6-PHOSPHATE; GLUCOSE-6-PHOSPHATE AND FRUCTOSE-6-PHOSPHATE; GLUCOSE-6-PHOSPHATE DEHYDROGENASE; GLYCELALDEHYDE-3-PHOSPHATE; GLYOXYLATE; GOX; HISTIDINE-PHOSPHORYLATABLE PROTEIN; HPR; ICDH; ICI; ICL; ISOCITRATE; ISOCITRATE DEHYDROGENASE; ISOCITRATE LYASE; MAL; MALATE; MALATE DEHYDROGENASE; MALATE SYNTHASE; MALIC ENZYME; MDH; MEZ; MODELING; MS; MULTIPLE CARBON SOURCES; OAA; OXALOACETATE; PCK; PDH; PENTOSE PHOSPHATE PATHWAY; PEP; PFK; PGDH; PHOSPHOENOL PYRUVATE; PHOSPHOENOLPYRUVATE CARBOXYKINASE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOSPHOENOLPYRUVATE SYNTHASE; PHOSPHOFRUCTOKINASE; PHOSPHOTRANSACETYLASE; PHOSPHOTRANSFERASE SYSTEM; PP PATHWAY; PPC; PPS; PTA; PTS; PYK; PYR; PYRUVATE; PYRUVATE DEHYDROGENASE; PYRUVATE KINASE; R5P; RIBOSE PHOSPHATE ISOMERASE; RIBOSE-5-PHOSPHATE; RIBULOSE PHOSPHATE EPIMERASE; RIBULOSE-5-PHOSPHATE; RPE; RPI; RU5P; S7P; SEDOHEPTULOSE-7-PHOSPHATE; SUC; SUCCINATE; SYSTEMS BIOLOGY; TAL; TCA CYCLE; TKTA; TKTB; TP; TRANSALDOLASE; TRANSKETOLASE I; TRANSKETOLASE II; TRICARBOXYLIC ACID CYCLE; TRIOSE PHOSPHATE; X5P; XT; XYI; XYK; XYL; XYLOSE; XYLOSE ISOMERASE; XYLOSE TRANSPORT; XYLU; XYLULOKINASE; XYLULOSE; XYLULOSE-5-PHOSPHATE; Α-KETOGLUTARATE; ΑKG;

ACETATES; CATABOLITE REPRESSION; CITRIC ACID CYCLE; COMPUTER SIMULATION; ESCHERICHIA COLI; FEEDBACK, PHYSIOLOGICAL; FERMENTATION; FRUCTOSEDIPHOSPHATES; GENE KNOCKOUT TECHNIQUES; GLUCOSE; GLYCOLYSIS; MODELS, BIOLOGICAL; PENTOSE PHOSPHATE PATHWAY; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASES; PYRUVATE KINASE; SYSTEMS BIOLOGY; XYLOSE;

EID: 84885847338     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2013.06.023     Document Type: Article

References (53)

1. Altintas M.M., Eddy C.K., Zhang M., McMillan J.D., Kompala D.S. Kinetic modeling to optimize pentose fermentation in Zymomonas mobilis. Biotechnology and Bioengineering 2006, 94:273-295.
2. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2006, (2006.0008).
3. Barkai N., Leibler S. Robustness in simple biochemical networks. Nature 1997, 387:913-917.
4. crr phosphorylation, and intracellular cyclic AMP levels in Escherichia coli K-12. Journal of Bacteriology 2007, 189:6891-6900.
5. Boris G. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nature Reviews Microbiology 2008, 6:613-624.
6. Bray D. Protein molecules as computational elements in living cells. Nature 1995, 376:307-312.
7. Chassagnole C., Noisommitt-Rizzi N., Schmid J.W., Mauch K., Reuss M. Dynamic modeling of the central carbon metabolism of Escherichia coli. Biotechnology and Bioengineering 2002, 79:53-73.
8. Cunningham D.S., Liu Z., Domagalski N., Koepsel R.R., Ataai M.M., Domach M.M. Pyruvate kinase-deficient Escherichia coli exhibits increased plasmid copy number and cyclic AMP levels. Journal of Bacteriology 2009, 191:3041-3049.
9. Dellomonaco C., Rivera C., Campbell P., Gonzalez R. Engineered respiro-fermentative metabolism for the production of biofuels and biochemicals from fatty acid-rich feedstocks. Applied and Environment Microbiology 2010, 76:5067-5078.
10. Eiteman M.A., Altman E. Overcoming acetate in Escherichia coli recombinant protein fermentations. Trends in Biotechnology 2006, 24:530-536.
11. Emmerling M., Dauner M., Ponti A., Fiaux J., Hochuli M., Szyperski T., Wuthrich K., Bailey J.E., Sauer U. Metabolic flux responses to pyruvate kinase knockout in Escherichia coli. Journal of Bacteriology 2002, 184:152-164.
12. Farmer W.R., Liao J.C. Reduction of aerobic acetate production by Escherichia coli. Applied and Environment Microbiology 1997, 63:3205-3210.
13. Görke B., Stülke J.R. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nature Reviews Microbiology 2008, 6:613-624.
14. Goyal S., Yuan J., Chen T., Rabinowitz J.D., Wingreen N.S. Achieving optimal growth through product feedback inhibition in metabolism. PLOS Computational Biology 2010, 6. 10.1371/journal.pcbi.1000802.
15. Hartwell L.H., Hopfield J.J., Leibler S., Murray A.W. From molecular to modular cell biology. Nature 1999, 402:C47-C52.
16. Hogema B.M., Arents J.C., Bader R., Eijkemans K., Yoshida H., Takahashi H., Aiba H., Postma P.W. 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. Molecular Microbiology 1998, 30:487-498.
17. Hutter S., Roche C.M., Blanch H.W., Clark D.S. Escherichia coli for biofuel production: bridging the gap from promise to practice. Trends in Biotechnology 2012, 30:538-545.
18. Ishii N., Nakahigashi K., Baba T., Robert M., Soga T., Kanai A., Hirasawa T., Naba M., Hirai K., Hoque A., Ho P.Y., Kakazu Y., Sugawara K., Igarashi S., Harada S., Masuda T., Sugiyama N., Togashi T., Hasegawa M., Takai Y., Yugi K., Arakawa K., Iwata N., Toya Y., Nakayama Y., Nishioka T., Shimizu K., Mori H., Tomita M. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 2007, 316:593-597.
19. Jensen E.B., Carlsen S. Production of recombinant human growth hormone in Escherichia coli: expression of different precursors and physiological effects of glucose, acetate, and salts. Biotechnology and Bioengineering 1990, 36:1-11.
20. Kadir T.A., Mannan A.A., Kierzek A.M., McFadden J., Shimizu K. Modeling and simulation of the main metabolism in Escherichia coli and its several single-gene knockout mutants with experimental verification. Microbial Cell Factories 2010, 9:88.
21. Kayser A., Weber J., Hecht V., Rinas U. Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 2005, 151:693-706.
22. Kim S.R., Ha S.J., Wei N., Oh E.J., Jin Y.S. Simultaneous co-fermentation of mixed sugars: a promising strategy for producing cellulosic ethanol. Trends in Biotechnology 2012, 30:274-282.
23. Kochanowski K., Volkmer B., Gerosa L., Haverkorn van Rijsewijk B.R., Schmidt A., Heinemann M. Functioning of a metabolic flux sensor in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:1130-1135.
24. Koh B.T., Nakashimada U., Pfeiffer M., Yap M.G.S. Comparison of acetate inhibition on growth of host and recombinant E. coli K12 strains. Biotechnology Letters 1992, 14:1115-1118.
25. Kotte O., Zaugg J.B., Heinemann M. Bacterial adaptation through distributed sensing of metabolic fluxes. Molecular Systems Biology 2010, 6:355.
26. Kremling A., Bettenbrock K., Gilles E.D. A feed-forward loop guarantees robust behavior in Escherichia coli carbohydrate uptake. Bioinformatics 2008, 24:704-710.
27. Kremling A., Fischer S., Sauter T., Bettenbrock K., Gilles E.D. Time hierarchies in the Escherichia coli carbohydrate uptake and metabolism. BioSystems 2004, 73:57-71.
28. Lee S.Y. High cell-density culture of Escherichia coli. Trends in Biotechnology 1996, 14:98-105.
29. Lin H., Castro N.M., Bennett G.N., San K.-Y. Acetyl-CoA synthetase overexpression in Escherichia coli demonstrates more efficient acetate assimilation and lower acetate accumulation: a potential tool in metabolic engineering. Applied Microbiology and Biotechnology 2006, 71:870-874.
30. Mailloux R.J., Bériault R., Lemire J., Singh R., Chénier D.R., Hamel R.D., Appanna V.D. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS ONE 2007, 2. 10.1371/journal.pone.0000690.
31. March J.C., Eiteman M.A., Altman E. Expression of an anaprelotic enzyme, pyruvate carboxylase improves recombinant protein production in Escherichia coli. Applied and Environment Microbiology 2002, 68:5620-5624.
32. Matsuoka Y., Shimizu K. Metabolic regulation in Escherichia coli in response to culture environments via global regulators. Biotechnology Journal 2011, 6:1330-1341.
33. Moat A.G., Foster J.W., Spector M.P. Microbial Pysiology 2002, A John Wiley & Sons, Inc. Publ., New York. 4th ed.
34. Nakano K., Rischke M., Sato S., Märkl H. Influence of acetic acid on the growth of Escherichia coli K12 during high-cell-density cultivation in a dialysis reactor. Applied Microbiology and Biotechnology 1997, 48:597-601.
35. Nanchen A., Schicker A., Sauer U. Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli. Applied and Environment Microbiology 2006, 72:1164-1172.
36. Park Y.H., Lee B.R., Seok Y.J., Peterkofsky A. In vitro reconstruction of catabolite repression in Escherichia coli. Journal of Biological Chemistry 2006, 281:6448-6454.
37. Peng L., Shimizu K. 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 2006, 38:512-520.
38. Plumbridge J. Expression of ptsG, the gene for the major glucose PTS transporter in Escherichia coli, is repressed by Mlc and induced by growth on glucose. Molecular Microbiology 1998, 29:1053-1063.
39. Ponce E., Martínez A., Bolívar F., Valle F. Stimulation of glucose catabolism through the pentose pathway by the absence of the two pyruvate kinase isoenzymes in Escherichia coli. Biotechnology and Bioengineering 1998, 58:292-295.
40. De Reuse H., Danchin A. The ptsH, ptsI and crr genes of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system: a complex operon with several modes of transcription. Journal of Bacteriology 1988, 179:3827-3837.
41. Saier M.H., Ramseier T.M. The catabolite repressor/activator (Cra) protein of enteric bacteria. Journal of Bacteriology 1996, 178:3411-3417.
42. Saier M.H., Ramseier T.M., Reizer J. Regulation of carbon utilization. Escherichia coli and Salmonella: cellular and molecular biology 1996, 1:1325-1343. ASM Press, Washington, D.C. 2nd ed.
43. Schmidt L.D., Dauenhauer P.J. Chemical engineering: hybrid routes to biofuels. Nature 2007, 447:914-915.
44. Shimizu K. Toward systematic metabolic engineering based on the analysis of metabolic regulation by the integration of different levels of information. Biochemical Engineering Journal 2009, 46:235-251.
45. Shimizu K. Bacterial cellular metabolic systems 2013, Woodhead Publishing Ltd, Oxford.
46. Siddiquee K.A., Arauzo-Bravo M.J., Shimizu K. Effect of a pyruvate kinase (pykF-gene) knockout mutation on the control of gene expression and metabolic fluxes in Escherichia coli. FEMS Microbiology Letters 2004, 235:25-33.
47. 13C-labeling experiments together with measurements of enzyme activities and intracellular metabolite concentrations. Applied Microbiology and Biotechnology 2004, 63:407-417.
48. Stelling J., Klamt S., Bettenbrock K., Schuster S., Gilles E.D. Metabolic network structure determines key aspects of functionality and regulation. Nature 2002, 420:190-193.
49. 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 2010, 26:975-992.
50. Valgepea K., Adamberg K., Nahku R., Lahtvee P.J., Arike L., Vilu R. Systems biology approach reveals that overflow metabolism of acetate in Escherichia coli is triggered by carbon catabolite repression of acetyl-CoA synthetase. BMC Systems Biology 2010, 4:166.
51. Wolfe A.J. The acetate switch. Microbiology and Molecular Biology Reviews 2005, 69:12-50.
52. Yang C., Hua Q., Baba T., Mori H., Shimizu K. 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 2003, 84:129-144.
53. Yao R., Hirose Y., Sarkar D., Nakahigashi K., Ye Q., Shimizu K. Catabolic regulation analysis of Escherichia coli and its crp, mlc, mgsA, pgi and ptsG mutants. Microbial Cell Factories 2011, 10:67.