Quantitative analysis of the fermentative metabolism of glycerol in Escherichia coli

Biotechnology and Bioengineering

Volumn 109, Issue 1, 2012, Pages 187-198

  Cintolesi, Angela ^a   Clomburg, James M ^a   Rigou, Venetia ^a   Zygourakis, Kyriacos ^a   Gonzalez, Ramon ^a  

^a Rice University   (United States)

Author keywords

Biofuels; Escherichia coli; Glycerol fermentation; Kinetic modeling; Metabolic control analysis

Indexed keywords

ANAEROBIC CONDITIONS; BATCH CULTURE; BIODIESEL PRODUCTION; CARBON SOURCE; CONTROL STRUCTURE; CRUDE GLYCEROL; DEGREE OF REDUCTION; DIHYDROXYACETONE; FLUX CONTROL COEFFICIENTS; GENETIC MANIPULATIONS; GLYCEROL DEHYDROGENASE; GLYCEROL FERMENTATION; GLYCOLYTIC FLUX; INDUSTRIAL SCALE; INTRACELLULAR METABOLITES; KINETIC EXPRESSION; KINETIC MODELING; MASS BALANCE; METABOLIC CONTROL; METABOLIC CONTROL ANALYSIS; OVER-EXPRESSION; PRODUCT SYNTHESIS; SIGNIFICANT IMPACTS;

BATCH CELL CULTURE; BIOFUELS; COMPUTER SIMULATION; ENZYMES; ESCHERICHIA COLI; ETHANOL; FERMENTATION; IGNEOUS ROCKS; KINETIC THEORY; KINETICS; METABOLISM; PHYSIOLOGY;

GLYCEROL;

ALCOHOL; GLYCEROL; GLYCEROL DEHYDROGENASE;

ALCOHOL PRODUCTION; ARTICLE; BACTERIAL METABOLISM; BACTERIUM CULTURE; BIOMASS; BIOSYNTHESIS; CELL GROWTH; ENZYME ACTIVITY; ESCHERICHIA COLI; FERMENTATION; GENE OVEREXPRESSION; GENETIC MANIPULATION; GLYCOLYSIS; METABOLIC REGULATION; METABOLITE; MOLECULAR MODEL; NONHUMAN; QUANTITATIVE ANALYSIS; SIMULATION;

BIOMASS; BIOREACTORS; ESCHERICHIA COLI; ETHANOL; FERMENTATION; GENE EXPRESSION; GLYCEROL; KINETICS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS;

ESCHERICHIA COLI;

EID: 81455143851     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23309     Document Type: Article

References (57)

1. Babul J, Clifton D, Kretschmer M, Fraenkel DG. 1993. Glucose metabolism in Escherichia coli and the effect of increased amount of aldolase. Biochemistry 32(17): 4685-4692.
2. Bachler C, Schneider P, Bahler P, Lustig A, Erni B. 2005. Escherichia coli dihydroxyacetone kinase controls gene expression by binding to transcription factor DhaR. EMBO J 24(2): 283-293.
3. Bakker BM, Michels PAM, Opperdoes FR, Westerhoff HV. 1997. Glycolysis in bloodstream form Trypanosoma brucei can be understood in terms of the kinetics of the glycolytic enzymes. J Biol Chem 272(6): 3207-3215.
4. Booth IR. 2005. Glycerol and methylglyoxal metabolism. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley N, Schaechter M, Umbarger HE, editors. Escherichia coli and Salmonella: Cellular and molecular biology (web edition). Washington, DC: ASM Press. Available at.
5. Britton HG, Carreras J, Grisolia S. 1972. Mechanism of yeast phosphoglycerate mutase. Biochemistry 11(16): 3008-3014.
6. Chassagnole C, Noisommit-Rizzi N, Schmid JW, Mauch K, Reuss M. 2002. Dynamic modeling of the central carbon metabolism of Escherichia coli. Biotechnol Bioeng 79(1): 53-73.
7. Clomburg JM, Gonzalez R. 2011. Metabolic engineering of Escherichia coli for the production of 1, 2-propanediol from glycerol. Biotechnol Bioeng 108(4): 867-879.
8. Dharmadi Y, Gonzalez R. 2005. A better global resolution function and a novel iterative stochastic search method for optimization of high-performance liquid chromatographic separation. J Chromatogr A 1070(1-2): 89-101.
9. Dharmadi Y, Murarka A, Gonzalez R. 2006. Anaerobic fermentation of glycerol by Escherichia coli: A new platform for metabolic engineering. Biotechnol Bioeng 94(5): 821-829.
10. Duggleby RG. 1994. Product inhibition of reversible enzyme-catalyzed reactions. Biochim Biophys Acta 1209(2): 238-240.
11. Durnin G, Clomburg J, Yeates Z, Alvarez PJJ, Zygourakis K, Campbell P, Gonzalez R. 2009. Understanding and harnessing the microaerobic metabolism of glycerol in Escherichia coli. Biotechnol Bioeng 103(1): 148-161.
12. Fell DA, Sauro HM. 1985. Metabolic control and its analysis. Additional relationships between elasticities and control coefficients. Eur J Biochem 148(3): 555-561.
13. Fifis T, Scopes RK. 1978. Purification of 3-phosphoglycerate kinase from diverse sources by affinity elution chromatography. Biochem J 175(1): 311-319.
14. Garcia V. 2002. Sensitivity analysis for ODEs and DAEs. Available at.
15. Gonzalez R, Murarka A, Dharmadi Y, Yazdani SS. 2008. A new model for the anaerobic fermentation of glycerol in enteric bacteria: Trunk and auxiliary pathways in Escherichia coli. Metab Eng 10(5): 234-245.
16. Gonzalez R, Campbell P, Wong M. 2010. Production of ethanol from thin stillage by metabolically engineered Escherichia coli. Biotechnol Lett 32(3): 405-411.
17. Grana X, Urena J, Ludevid D, Carreras J, Climent F. 1989. Purification, characterization and immunological properties of 2, 3-bisphosphoglycerate-independent phosphoglycerate mutase from maize (zea-mays) seeds. Eur J Biochem 186(1-2): 149-153.
18. Gutknecht R, Beutler R, Garcia-Alles LF, Baumann U, Erni B. 2001. The dihydroxyacetone kinase of Escherichia coli utilizes a phosphoprotein instead of ATP as phosphoryl donor. EMBO J 20(10): 2480-2486.
19. Heller KB, Lin EC, Wilson TH. 1980. Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol 144: 274-278.
20. Hoefnagel MHN, Starrenburg MJC, Martens DE, Hugenholtz J, Kleerebezem M, Van Swam II, Bongers R, Westerhoff HV, Snoep JL. 2002. Metabolic engineering of lactic acid bacteria, the combined approach: Kinetic modelling, metabolic control and experimental analysis. Microbiology 148: 1003-1013.
21. Hofmeyr JHS, Kacser H, Vandermerwe KJ. 1986. Metabolic control analysis of moiety-conserved cycles. Eur J Biochem 155(3): 631-641.
22. Hu HB, Wood TK. 2010. An evolved Escherichia coli strain for producing hydrogen and ethanol from glycerol. Biochem Biophys Res Commun 391(1): 1033-1038.
23. Kang YS, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR. 2004. Systematic mutagenesis of the Escherichia coli genome (vol 186, pg 4921, 2004). J Bacteriol 186(24): 8548-8548.
24. Khanal SK, Rasmussen M, Shrestha P, Van Leeuwen H, Visvanathan C, Liu H. 2008. Bioenergy and biofuel production from wastes/residues of emerging biofuel industries. Water Environ Res 80(10): 1625-1647.
25. Kleinhans FW. 1998. Membrane permeability modeling: Kedem-Katchalsky vs a two-parameter formalism. Cryobiology 37(4): 271-289.
26. Knappe J, Blaschkowski HP, Grobner P, Schmitt T. 1974. Pyruvate formate-lyase of Escherichia coli: The acetyl-enzyme intermediate. Eur J Biochem 50(1): 253-263.
27. Koebmann BJ, Westerhoff HV, Snoep JL, Nilsson D, Jensen PR. 2002. The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J Bacteriol 184(14): 3909-3916.
28. Kornberg HL, Reeves RE. 1972. Inducible phosphoenolpyruvate-dependent hexose phosphotransferase activities in Escherichia coli. Biochem J 128(5): 1339-1344.
29. Lavoinne A, Marchand JC, Chedeville A, Matray F. 1983. Kinetic-studies of the reaction-mechanism of rat-liver phosphoglycerate kinase in the direction of ADP utilization. Biochimie 65(3): 211-220.
30. Lu DY, Grayson P, Schulten K. 2003. Glycerol conductance and physical asymmetry of the Escherichia coli glycerol facilitator GlpF. Biophys J 85(5): 2977-2987.
31. Membrillo-Hernandez J, Echave P, Cabiscol E, Tamarit J, Ros J, Lin ECC. 2000. Evolution of the adhE gene product of Escherichia coli from a functional reductase to a dehydrogenase-Genetic and biochemical studies of the mutant proteins. J Biol Chem 275(43): 33869-33875.
32. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
33. Molnar M, Vas M. 1993. Mg2+ affects the binding of ADP but not ATP to 3-phosphoglycerate kinase. Correlation between equilibrium dialysis binding and enzyme-kinetic data. Biochem J 293: 595-599.
34. Murarka A, Dharmadi Y, Yazdani SS, Gonzalez R. 2008. Fermentative utilization of glycerol by Escherichia coli and its implications for the production of fuels and chemicals. Appl Environ Microbiol 74(4): 1124-1135.
35. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J Bacteriol 119(3): 736-747.
36. Ni TC, Savageau MA. 1996. Model assessment and refinement using strategies from biochemical systems theory: Application to metabolism in human red blood cells. J Theor Biol 179(4): 329-368.
37. Nikel PI, Ramirez MC, Pettinari MJ, Mendez BS, Galvagno MA. 2010. Ethanol synthesis from glycerol by Escherichia coli redox mutants expressing adhE from Leuconostoc mesenteroides. J Appl Microbiol 109(2): 492-504.
38. Pettersson G. 1990. What metabolite levels may be evolutionarily reached in the glycolytic pathway. Eur J Biochem 194(1): 141-146.
39. Rausch KD, Belyea RL. 2006. The future of coproducts from corn processing. Appl Biochem Biotechnol 128(1): 47-86.
40. Richter O, Betz A, Giersch C. 1975. Response of oscillating glycolysis to perturbations in NADH/NAD system. A comparison between experiments and a computer model. Biosystems 7(1): 137-146.
41. Romeo T, Snoep JL. 2005. Glycolysis and flux control. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley N, Schaechter M, Umbarger HE, editors. Escherichia coli and Salmonella: Cellular and molecular biology (web edition). Washington, DC: ASM Press. Available at.
42. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
43. Sawers RG, Clark DP. 2004. Fermentative pyruvate and acetyl-coenzyme A metabolism. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley N, Schaechter M, Umbarger HE, editors. Escherichia coli and Salmonella: Cellular and molecular biology (web edition). Washington, DC: ASM Press. Available at.
44. Schaub J, Reuss M. 2008. In vivo dynamics of glycolysis in Escherichia coli shows need for growth-rate dependent metabolome analysis. Biotechnol Prog 24(6): 1402-1407.
45. Schmidt PP, Travers F, Barman T. 1995. Transient and equilibrium kinetic-studies on yeast 3-phosphoglycerate kinase. Evidence that an intermediate containing 1, 3-bisphosphoglycerate accumulates in the steady-state. Biochemistry 34(3): 824-832.
46. Shone CC, Fromm HJ. 1981. Steady-state and pre-steady-state kinetics of coenzyme A linked aldehyde dehydrogenase from Escherichia coli. Biochemistry 20(26): 7494-7501.
47. Spring TG, Wold F. 1971. Purification and characterization of Escherichia coli enolase. J Biol Chem 246(22): 6797-6802.
48. Stephanopoulos GN, Aristidou AA, Nielsen J. 1998. Metabolic engineering: Principles and methodologies. San Diego, CA: Academic Press.
49. Subedi KP, Kim I, Kim J, Min B, Park C. 2008. Role of GldA in dihydroxyacetone and methylglyoxal metabolism of Escherichia coli K12. FEMS Microbiol Lett 279(2): 180-187.
50. Sundararaj S, Guo A, Habibi-Nazhad B, Rouani M, Stothard P, Ellison M, Wishart DS. 2004. The CyberCell Database (CCDB): a comprehensive, self-updating relational database to coordinate and facilitate in silico modeling of Escherichia coli. Nucleic Acids Res 32: D293-D295.
51. Trinh CT, Srienc F. 2009. Metabolic engineering of Escherichia coli for efficient conversion of glycerol to ethanol. Appl Environ Microbiol 75(21): 6696-6705.
52. Voegele RT, Sweet GD, Boos W. 1993. Glycerol kinase of Escherichia coli is activated by interaction with the glycerol facilitator. J Bacteriol 175(4): 1087-1094.
53. Yazdani SS, Gonzalez R. 2007. Anaerobic fermentation of glycerol: A path to economic viability for the biofuels industry. Curr Opin Biotechnol 18(3): 213-219.
54. Yazdani SS, Gonzalez R. 2008. Engineering Escherichia coli for the efficient conversion of glycerol to ethanol and co-products. Metab Eng 10(6): 340-351.
55. Zhang XL, Shanmugam KT, Ingram LO. 2010. Fermentation of glycerol to succinate by metabolically engineered strains of Escherichia coli. Appl Environ Microbiol 76(8): 2397-2401.
56. Zhu J, Shimizu K. 2004. The effect of pfl gene knockout on the metabolism for optically pure D-lactate production by Escherichia coli. Appl Microbiol Biotechnol 64(3): 367-375.
57. Zhu YH, Eiteman MA, Lee SA, Altman E. 2010. Conversion of glycerol to pyruvate by Escherichia coli using acetate- and acetate/glucose-limited fed-batch processes. J Ind Microbiol Biotechnol 37(3): 307-312.