Pathway Thermodynamics Highlights Kinetic Obstacles in Central Metabolism

PLoS Computational Biology

Volumn 10, Issue 2, 2014, Pages

  Noor, Elad ^a   Bar Even, Arren ^a   Flamholz, Avi ^a,b   Reznik, Ed ^c   Liebermeister, Wolfram ^d   Milo, Ron ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Berkeley   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ENZYMES; IONIC STRENGTH; KINETICS; METABOLISM; PHYSIOLOGY; REACTION KINETICS;

CATALYSE; CENTRAL METABOLISMS; DRIVING FORCES; ENZYME CATALYSIS; MAX/MIN; REVERSE FLUXES; REVERSE REACTIONS; THERMODYNAMIC DRIVING FORCES; THERMODYNAMIC POTENTIALS; THERMODYNAMICS FLUXES;

THERMODYNAMICS;

CITRATE SYNTHASE; MALATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXALOACETIC ACID; QUINONE DERIVATIVE; ENZYME;

ARTICLE; CELL PH; CONCENTRATION (PARAMETERS); CONCEPTUAL FRAMEWORK; ENZYME ACTIVITY; ENZYME CHEMISTRY; ENZYME KINETICS; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; FERMENTATION; IONIC STRENGTH; METABOLITE; NONHUMAN; THERMODYNAMICS; BIOLOGICAL MODEL; BIOLOGY; CITRIC ACID CYCLE; ESCHERICHIA COLI; KINETICS; METABOLISM; OSMOLARITY; PHOSPHORYLATION;

CITRIC ACID CYCLE; COMPUTATIONAL BIOLOGY; ENZYMES; ESCHERICHIA COLI; FERMENTATION; KINETICS; MALATE DEHYDROGENASE; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; OSMOLAR CONCENTRATION; PHOSPHORYLATION; THERMODYNAMICS;

EID: 84895727036     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003483     Document Type: Article

References (103)

1. Heinrich R, Montero F, Klipp E, Waddell TG, Melendez-Hevia E, (1997) Theoretical approaches to the evolutionary optimization of glycolysis: thermodynamic and kinetic constraints. Eur J Biochem 243: 191-201.
2. Melendez-Hevia E, Waddell TG, Heinrich R, Montero F, (1997) Theoretical approaches to the evolutionary optimization of glycolysis-chemical analysis. Eur J Biochem 244: 527-543.
3. Stephani A, Nuno JC, Heinrich R, (1999) Optimal stoichiometric designs of ATP-producing systems as determined by an evolutionary algorithm. J Theor Biol 199: 45-61.
4. Ebenhoh O, Heinrich R, (2001) Evolutionary optimization of metabolic pathways. Theoretical reconstruction of the stoichiometry of ATP and NADH producing systems. Bull Math Biol 63: 21-55.
5. Segre D, Vitkup D, Church GM, (2002) Analysis of optimality in natural and perturbed metabolic networks. Proc Natl Acad Sci U S A 99: 15112-15117.
6. Schuster S, Pfeiffer T, Fell DA, (2008) Is maximization of molar yield in metabolic networks favoured by evolution? J Theor Biol 252: 497-504.
7. Molenaar D, van Berlo R, de Ridder D, Teusink B, (2009) Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol 5: 323.
8. Noor E, Eden E, Milo R, Alon U, (2010) Central carbon metabolism as a minimal biochemical walk between precursors for biomass and energy. Mol Cell 39: 809-820.
9. Bar-Even A, Flamholz A, Noor E, Milo R, (2012) Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim Biophys Acta 1817: 1646-1659.
10. Bar-Even A, Flamholz A, Noor E, Milo R, (2012) Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nat Chem Biol 8: 509-517.
11. Bar-Even A, Noor E, Milo R, (2012) A survey of carbon fixation pathways through a quantitative lens. J Exp Bot 63: 2325-2342.
12. Schuetz R, Zamboni N, Zampieri M, Heinemann M, Sauer U, (2012) Multidimensional optimality of microbial metabolism. Science 336: 601-604.
13. Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R, (2013) Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc Natl Acad Sci U S A 110: 10039-10044.
14. Bar-Even A, Noor E, Lewis NE, Milo R, (2010) Design and analysis of synthetic carbon fixation pathways. Proc Natl Acad Sci U S A 107: 8889-8894.
15. Vojinovic V, von Stockar U, (2009) Influence of uncertainties in pH, pMg, activity coefficients, metabolite concentrations, and other factors on the analysis of the thermodynamic feasibility of metabolic pathways. Biotechnol Bioeng 103: 780-795.
16. von Stockar U, Maskow T, Liu J, Marison IW, Patino R, (2006) Thermodynamics of microbial growth and metabolism: an analysis of the current situation. J Biotechnol 121: 517-533.
17. Hatzimanikatis V, Li C, Ionita JA, Henry CS, Jankowski MD, et al. (2005) Exploring the diversity of complex metabolic networks. Bioinformatics 21: 1603-1609.
18. Finley SD, Broadbelt LJ, Hatzimanikatis V, (2009) Thermodynamic analysis of biodegradation pathways. Biotechnol Bioeng 103: 532-541.
19. Miskovic L, Hatzimanikatis V, (2010) Production of biofuels and biochemicals: in need of an ORACLE. Trends Biotechnol 28: 391-397.
20. Bar-Even A, Noor E, Flamholz A, Milo R, (2013) Design and analysis of metabolic pathways supporting formatotrophic growth for electricity-dependent cultivation of microbes. Biochim Biophys Acta 1827: 1039-1047.
21. Beard DA, Qian H, (2005) Thermodynamic-based computational profiling of cellular regulatory control in hepatocyte metabolism. Am J Physiol Endocrinol Metab 288: E633-644.
22. Noor E, Bar-Even A, Flamholz A, Lubling Y, Davidi D, et al. (2012) An integrated open framework for thermodynamics of reactions that combines accuracy and coverage. Bioinformatics 28: 2037-2044.
23. Beard DA, Qian H, (2007) Relationship between thermodynamic driving force and one-way fluxes in reversible processes. PLoS One 2: e144.
24. Rottenberg H, (1973) The thermodynamic description of enzyme-catalyzed reactions. The linear relation between the reaction rate and the affinity. Biophys J 13: 503-511.
25. Van Der Meer R, Westerhoff HV, Van Dam K, (1980) Linear relation between rate and thermodynamic force in enzyme-catalyzed reactions. Biochim Biophys Acta 591: 488-493.
26. Kacser H, Burns JA, (1973) The control of flux. Symp Soc Exp Biol 27: 65-104.
27. Westerhoff HV (1987) Thermodynamics and Control of Biological Free-Energy Transduction: Elsevier Science Ltd.
28. Acerenza L, (1993) Metabolic control design. J Theor Biol 165: 63-85.
29. Crabtree B, Newsholme EA, Reppas NB (1997) Principles of regulation and control in biochemistry: a pragmatic, flux-oriented approach. In: Hoffman JF, Jamieson JD, editors. Handbook of Physiology. New York, USA: Oxford University Press.pp. 117-180.
30. Nielsen J, (1997) Metabolic control analysis of biochemical pathways based on a thermokinetic description of reaction rates. Biochem J 321 (Pt 1): 133-138.
31. Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, et al. (2011) The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50: 4402-4410.
32. Noor E, Haraldsdottir HS, Milo R, Fleming RMT, (2013) Consistent estimation of GIbbs energy using component contributions. Plos Comp Biol 9: e1003098.
33. Alberty RA (2003) Thermodynamics of Biochemical Reactions: Wiley-Interscience.
34. Alberty RA, (2006) Biochemical thermodynamics: applications of Mathematica. Methods Biochem Anal 48: 1-458.
35. Goldberg RN, Tewari YB, Bhat TN, (2004) Thermodynamics of enzyme-catalyzed reactions-a database for quantitative biochemistry. Bioinformatics 20: 2874-2877.
36. Goldberg RN, Tewari YB, Bhat TN, (2007) Thermodynamics of enzyme-catalyzed reactions: Part 7-2007 update J Phys Chem Ref Data. 36: 1347-1397.
37. Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 55: 1-79, 317.
38. McNaught AD, Wilkinson A (1997) Compendium of Chemical Terminology, 2nd ed. (the IUPAC "Gold Book"). Oxford: Blackwell Scientific Publications.
39. Alberty RA, (1996) Calculation of biochemical net reactions and pathways by using matrix operations. Biophys J 71: 507-515.
40. Brochado AR, Andrejev S, Maranas CD, Patil KR, (2012) Impact of stoichiometry representation on simulation of genotype-phenotype relationships in metabolic networks. PLoS Comput Biol 8: e1002758.
41. Mavrovouniotis ML, (1993) Identification of localized and distributed bottlenecks in metabolic pathways. Proc Int Conf Intell Syst Mol Biol 1: 275-283.
42. Kelly FP, Maulloo AK, Tan DKH, (1998) Rate control for communication networks: shadow prices, proportional fairness and stability. J Oper Res Soc 49: 237-252.
43. Bertsimas D, Tsitsiklis JN, Tsitsiklis J (1997) Introduction to Linear Optimization.
44. Bar-Even A, Noor E, Flamholz A, Buescher JM, Milo R, (2011) Hydrophobicity and charge shape cellular metabolite concentrations. PLoS Comput Biol 7: e1002166.
45. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, et al. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5: 593-599.
46. Zampar GG, Kummel A, Ewald J, Jol S, Niebel B, et al. (2013) Temporal system-level organization of the switch from glycolytic to gluconeogenic operation in yeast. Mol Syst Biol 9: 651.
47. Ugurbil K, Rottenberg H, Glynn P, Shulman RG, (1982) Phosphorus-31 nuclear magnetic resonance studies of bioenergetics in wild-type and adenosinetriphosphatase(1-) Escherichia coli cells. Biochemistry 21: 1068-1075.
48. 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: 3909-3916.
49. Ishii N, Nakahigashi K, Baba T, Robert M, Soga T, et al. (2007) Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316: 593-597.
50. de Graef MR, Alexeeva S, Snoep JL, Teixeira de Mattos MJ, (1999) The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. J Bacteriol 181: 2351-2357.
51. Bautista J, Satrustegui J, Machado A, (1979) Evidence suggesting that the NADPH/NADP ratio modulates the splitting of the isocitrate flux between the glyoxylic and tricarboxylic acid cycles, in Escherichia coli. FEBS Lett 105: 333-336.
52. Stiefel EI, George GN (1994) Ferredoxins, Hydrogenases, and Nitrogenases: Metal-Sulfide Proteins. Bioinorganic Chemistry. pp. 365-453.
53. Ugurbil K, Rottenberg H, Glynn P, Shulman RG, (1978) 31P nuclear magnetic resonance studies of bioenergetics and glycolysis in anaerobic Escherichia coli cells. Proc Natl Acad Sci U S A 75: 2244-2248.
54. Xavier KB, Kossmann M, Santos H, Boos W, (1995) Kinetic analysis by in vivo 31P nuclear magnetic resonance of internal Pi during the uptake of sn-glycerol-3-phosphate by the pho regulon-dependent Ugp system and the glp regulon-dependent GlpT system. J Bacteriol 177: 699-704.
55. Moreau PL, Gerard F, Lutz NW, Cozzone P, (2001) Non-growing Escherichia coli cells starved for glucose or phosphate use different mechanisms to survive oxidative stress. Mol Microbiol 39: 1048-1060.
56. Chen J, Brevet A, Fromant M, Leveque F, Schmitter JM, et al. (1990) Pyrophosphatase is essential for growth of Escherichia coli. J Bacteriol 172: 5686-5689.
57. Stockbridge RB, Wolfenden R, (2011) Enhancement of the rate of pyrophosphate hydrolysis by nonenzymatic catalysts and by inorganic pyrophosphatase. J Biol Chem 286: 18538-18546.
58. Fell D (1996) Understanding the Control of Metabolism: Portland Pr.
59. Klipp E, Liebermeister W, Wierling C, Kowald A, Lehrach H, et al. (2009) Systems Biology: Wiley-Blackwell.
60. Haldane JBS (1930) Enzymes. London: Longmans & Green.
61. Noor E, Flamholz A, Liebermeister W, Bar-Even A, Milo R, (2013) A note on the kinetics of enzyme action: A decomposition that highlights thermodynamic effects. FEBS Lett 587: 2772-2777.
62. O'Boyle NM, Banck M, James CA, Morley C, Vandermeersch T, et al. (2011) Open Babel: An open chemical toolbox. J Cheminform 3: 33.
63. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480-484.
64. Fischer E, Sauer U, (2003) A novel metabolic cycle catalyzes glucose oxidation and anaplerosis in hungry Escherichia coli. J Biol Chem 278: 46446-46451.
65. Chen X, Alonso AP, Allen DK, Reed JL, Shachar-Hill Y, (2011) Synergy between (13)C-metabolic flux analysis and flux balance analysis for understanding metabolic adaptation to anaerobiosis in E. coli. Metab Eng 13: 38-48.
66. Wright BE, Butler MH, Albe KR, (1992) Systems analysis of the tricarboxylic acid cycle in Dictyostelium discoideum. I. The basis for model construction. J Biol Chem 267: 3101-3105.
67. Ringe D, Petsko GA, (2008) Biochemistry. How enzymes work. Science 320: 1428-1429.
68. Weber AL, (2004) Kinetics of organic transformations under mild aqueous conditions: implications for the origin of life and its metabolism. Orig Life Evol Biosph 34: 473-495.
69. Pharkya P, Nikolaev EV, Maranas CD, (2003) Review of the BRENDA Database. Metab Eng 5: 71-73.
70. Datta A, Merz JM, Spivey HO, (1985) Substrate channeling of oxalacetate in solid-state complexes of malate dehydrogenase and citrate synthase. J Biol Chem 260: 15008-15012.
71. Tompa P, Batke J, Ovadi J, Welch GR, Srere PA, (1987) Quantitation of the interaction between citrate synthase and malate dehydrogenase. J Biol Chem 262: 6089-6092.
72. Srere PA, (1987) Complexes of sequential metabolic enzymes. Annu Rev Biochem 56: 89-124.
73. Morgunov I, Srere PA, (1998) Interaction between citrate synthase and malate dehydrogenase. Substrate channeling of oxaloacetate. J Biol Chem 273: 29540-29544.
74. Bar-Even A, (2013) Does acetogenesis really require especially low reduction potential? Biochim Biophys Acta 1827: 395-400.
75. van der Rest ME, Frank C, Molenaar D, (2000) Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Escherichia coli. J Bacteriol 182: 6892-6899.
76. Kather B, Stingl K, van der Rest ME, Altendorf K, Molenaar D, (2000) Another unusual type of citric acid cycle enzyme in Helicobacter pylori: the malate:quinone oxidoreductase. J Bacteriol 182: 3204-3209.
77. Molenaar D, van der Rest ME, Drysch A, Yucel R, (2000) Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Corynebacterium glutamicum. J Bacteriol 182: 6884-6891.
78. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci U S A 100: 10020-10025.
79. Forster-Fromme K, Jendrossek D, (2005) Malate:quinone oxidoreductase (MqoB) is required for growth on acetate and linear terpenes in Pseudomonas citronellolis. FEMS Microbiol Lett 246: 25-31.
80. Sweetlove LJ, Beard KF, Nunes-Nesi A, Fernie AR, Ratcliffe RG, (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15: 462-470.
81. Singh R, Lemire J, Mailloux RJ, Chenier D, Hamel R, et al. (2009) An ATP and oxalate generating variant tricarboxylic acid cycle counters aluminum toxicity in Pseudomonas fluorescens. PLoS One 4: e7344.
82. Noguchi Y, Nakai Y, Shimba N, Toyosaki H, Kawahara Y, et al. (2004) The energetic conversion competence of Escherichia coli during aerobic respiration studied by 31P NMR using a circulating fermentation system. J Biochem 136: 509-515.
83. Sung SJS, Xu DP, Galloway CM, Black CCJ, (1988) A reassessment of glycolysis and gluconeogenesis in higher plants. Physiol Plant 72: 650-654.
84. Verhees CH, Kengen SW, Tuininga JE, Schut GJ, Adams MW, et al. (2003) The unique features of glycolytic pathways in Archaea. Biochem J 375: 231-246.
85. Kalapos MP, (1999) Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications. Toxicol Lett 110: 145-175.
86. Zhang X, Harrison DH, Cui Q, (2002) Functional specificities of methylglyoxal synthase and triosephosphate isomerase: a combined QM/MM analysis. J Am Chem Soc 124: 14871-14878.
87. Hopper DJ, Cooper RA, (1971) The regulation of Escherichia coli methylglyoxal synthase; a new control site in glycolysis? FEBS Lett 13: 213-216.
88. Siebers B, Schonheit P, (2005) Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr Opin Microbiol 8: 695-705.
89. Ahmed H, Ettema TJ, Tjaden B, Geerling AC, van der Oost J, et al. (2005) The semi-phosphorylative Entner-Doudoroff pathway in hyperthermophilic archaea: a re-evaluation. Biochem J 390: 529-540.
90. Sonderegger M, Schumperli M, Sauer U, (2004) Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl Environ Microbiol 70: 2892-2897.
91. Bogorad IW, Lin TS, Liao JC (2013) Synthetic non-oxidative glycolysis enables complete carbon conservation. Nature.
92. Noor E, Milo R, (2012) Evolution. Efficiency in evolutionary trade-offs. Science 336: 1114-1115.
93. Alexeeva S, de Kort B, Sawers G, Hellingwerf KJ, de Mattos MJ, (2000) Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli. J Bacteriol 182: 4934-4940.
94. Levanon SS, 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.
95. Zhu J, Shalel-Levanon S, Bennett G, San KY, (2007) The YfiD protein contributes to the pyruvate formate-lyase flux in an Escherichia coli arcA mutant strain. Biotechnol Bioeng 97: 138-143.
96. Link H, Kochanowski K, Sauer U, (2013) Systematic identification of allosteric protein-metabolite interactions that control enzyme activity in vivo. Nat Biotechnol 31: 357-361.
97. Ruzanski C, Smirnova J, Rejzek M, Cockburn D, Pedersen HL, et al. (2013) A bacterial glucanotransferase can replace the complex maltose metabolism required for starch to sucrose conversion in leaves at night. J Biol Chem 288: 28581-28598.
98. Kartal O, Mahlow S, Skupin A, Ebenhoh O, (2011) Carbohydrate-active enzymes exemplify entropic principles in metabolism. Mol Syst Biol 7: 542.
99. Fersht A (1998) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. New York: W. H. Freeman.
100. Visser D, Schmid JW, Mauch K, Reuss M, Heijnen JJ, (2004) Optimal re-design of primary metabolism in Escherichia coli using linlog kinetics. Metab Eng 6: 378-390.
101. Wang L, Birol I, Hatzimanikatis V, (2004) Metabolic control analysis under uncertainty: framework development and case studies. Biophys J 87: 3750-3763.
102. Kummel A, Panke S, Heinemann M (2006) Putative regulatory sites unraveled by network-embedded thermodynamic analysis of metabolome data. Mol Syst Biol 22006 0034.
103. Schramm M, Klybas V, Racker E, (1958) Phosphorolytic cleavage of fructose-6-phosphate by fructose-6-phosphate phosphoketolase from Acetobacter xylinum. J Biol Chem 233: 1283-1288.