Succinate Overproduction: A Case Study of Computational Strain Design Using a Comprehensive Escherichia coli Kinetic Model

Frontiers in Bioengineering and Biotechnology

Volumn 2, Issue , 2015, Pages

  Khodayari, Ali ^a   Chowdhury, Anupam ^a   Maranas, Costas D ^a  

^a The Pennsylvania State University   (United States)

Author keywords

bilevel optimization; computational strain design; kinetic model; model parameterization; succinate overproduction

Indexed keywords

ESCHERICHIA COLI; FORECASTING; KINETIC THEORY; METABOLISM; PARAMETERIZATION; PHYSIOLOGY;

ANAEROBIC CONDITIONS; BI-LEVEL OPTIMIZATION; CASE-STUDIES; COMPUTATIONAL STRAIN DESIGN; ENVIRONMENTAL PERTURBATIONS; KINETIC MODELS; MODEL PARAMETERIZATION; MODEL PREDICTION; PARAMETERIZED; SUCCINATE OVERPRODUCTION;

KINETIC PARAMETERS;

EID: 85117273619     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2014.00076     Document Type: Article

References (73)

1. Almquist J. Cvijovic M. Hatzimanikatis V. Nielsen J. Jirstrand M. (2014). Kinetic models in industrial biotechnology – improving cell factory performance. Metab. Eng. 24, 38–60.10.1016/j.ymben.2014.03.007
2. Angermayr S. A. Hellingwerf K. J. (2013). On the use of metabolic control analysis in the optimization of cyanobacterial biosolar cell factories. J. Phys. Chem. B 117, 11169–11175.10.1021/jp4013152
3. Baez-Viveros J. L. Flores N. Juarez K. Castillo-Espana P. Bolivar F. Gosset G. (2007). Metabolic transcription analysis of engineered Escherichia coli strains that overproduce L-phenylalanine. Microb. Cell Fact. 6, 30.10.1186/1475-2859-6-30
4. Burgard A. P. Pharkya P. Maranas C. D. (2003). Optknock: a bilevel programming framework for identifying gene knockout strategies for microbial strain optimization. Biotechnol. Bioeng. 84, 647–657.10.1002/bit.10803
5. Cao Y. Cao Y. Lin X. (2011). Metabolically engineered Escherichia coli for biotechnological production of four-carbon 1,4-dicarboxylic acids. J. Ind. Microbiol. Biotechnol. 38, 649–656.10.1007/s10295-010-0913-4
6. Cao Y. Zhang R. Sun C. Cheng T. Liu Y. Xian M. (2013). Fermentative succinate production: an emerging technology to replace the traditional petrochemical processes. Biomed Res. Int. 2013, 723412.10.1155/2013/723412
7. Cho B. K. Knight E. M. Palsson B. O. (2006). Transcriptional regulation of the fad regulon genes of Escherichia coli by ArcA. Microbiology 152, 2207–2219.10.1099/mic.0.28912-0
8. Choudhary M. K. Yoon J. M. Gonzalez R. Shanks J. V. (2011). Re-examination of metabolic fluxes in Escherichia coli during anaerobic fermentation of glucose using C-13 labeling experiments and 2-dimensional nuclear magnetic resonance (NMR) spectroscopy. Biotechnol. Bioprocess Eng. 16, 419–437.10.1007/s12257-010-0449-5
9. Chowdhury A. Zomorrodi A. R. Maranas C. D. (2014). k-OptForce: integrating kinetics with flux balance analysis for strain design. PLoS Comput. Biol. 10:e1003487.10.1371/journal.pcbi.1003487
10. Cotten C. Reed J. L. (2013a). Constraint-based strain design using continuous modifications (CosMos) of flux bounds finds new strategies for metabolic engineering. Biotechnol. J. 8, 595–604.10.1002/biot.201200316
11. Cotten C. Reed J. L. (2013b). Mechanistic analysis of multi-omics datasets to generate kinetic parameters for constraint-based metabolic models. BMC Bioinformatics 14:32.10.1186/1471-2105-14-32
12. Curran K. A. Alper H. S. (2012). Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metab. Eng. 14, 289–297.10.1016/j.ymben.2012.04.006
13. Duckworth H. W. Barber B. H. Sanwal B. D. (1973). The interaction of phosphoglucomutase with nucleotide inhibitors. J. Biol. Chem. 248, 1431–1435.
14. Feist A. M. Henry C. S. Reed J. L. Krummenacker M. Joyce A. R. Karp P. D. et al. (2007). A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3, 121.10.1038/msb4100155
15. Feng X. Xu Y. Chen Y. Tang Y. J. (2012). Integrating flux balance analysis into kinetic models to decipher the dynamic metabolism of Shewanella oneidensis MR-1. PLoS Comput. Biol. 8:e1002376.10.1371/journal.pcbi.1002376
16. Fleming R. M. Thiele I. Provan G. Nasheuer H. P. (2010). Integrated stoichiometric, thermodynamic and kinetic modelling of steady state metabolism. J. Theor. Biol. 264, 683–692.10.1016/j.jtbi.2010.02.044
17. Flowers D. Thompson R. A. Birdwell D. Wang T. Trinh C. T. (2013). SMET: systematic multiple enzyme targeting – a method to rationally design optimal strains for target chemical overproduction. Biotechnol. J. 8, 605–618.10.1002/biot.201200233
18. Grant G. A. (2012). Contrasting catalytic and allosteric mechanisms for phosphoglycerate dehydrogenases. Arch. Biochem. Biophys. 519, 175–185.10.1016/j.abb.2011.10.005
19. Grossmann I. E. Viswanathan J. Vecchietti A. Raman R. Kalvelagen E. (2002). GAMS/DICOPT: A Discrete Continuous Optimization Package. Washington, DC: GAMS Development Corporation.
20. Gruys K. J. Walker M. C. Sikorski J. A. (1992). Substrate synergism and the steady-state kinetic reaction mechanism for EPSP synthase from Escherichia coli. Biochemistry 31, 5534–5544.10.1021/bi00139a016
21. Heijnen J. J. Verheijen P. J. (2013). Parameter identification of in vivo kinetic models: limitations and challenges. Biotechnol. J. 8, 768–775.10.1002/biot.201300105
22. Hong K. K. Nielsen J. (2012). Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries. Cell. Mol. Life Sci. 69, 2671–2690.10.1007/s00018-012-0945-1
23. Hoyt J. C. Robertson E. F. Berlyn K. A. Reeves H. C. (1988). Escherichia coli isocitrate lyase: properties and comparisons. Biochim. Biophys. Acta 966, 30–35.10.1016/0304-4165(88)90125-0
24. Hubbard B. K. Koch M. Palmer D. R. Babbitt P. C. Gerlt J. A. (1998). Evolution of enzymatic activities in the enolase superfamily: characterization of the (D)-glucarate/galactarate catabolic pathway in Escherichia coli. Biochemistry 37, 14369–14375.10.1021/bi981124f
25. Ishii N. Nakahigashi K. Baba T. Robert M. Soga T. Kanai A. et al. (2007). Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316, 593–597.10.1126/science.1132067
26. Jamshidi N. Palsson B. O. (2010). Mass action stoichiometric simulation models: incorporating kinetics and regulation into stoichiometric models. Biophys. J. 98, 175–185.10.1016/j.bpj.2009.09.064
27. Jouhten P. (2012). Metabolic modelling in the development of cell factories by synthetic biology. Comput. Struct. Biotechnol. J. 3, 9.10.5936/csbj.201210009
28. Khodayari A. Zomorrodi A. R. Liao J. C. Maranas C. D. (2014). A kinetic model of Escherichia coli core metabolism satisfying multiple sets of mutant flux data. Metab. Eng. 25C, 50–62.10.1016/j.ymben.2014.05.014
29. Kim J. Reed J. L. (2010). OptORF: optimal metabolic and regulatory perturbations for metabolic engineering of microbial strains. BMC Syst. Biol. 4:53.10.1186/1752-0509-4-53
30. Kim J. Reed J. L. Maravelias C. T. (2011). Large-scale bi-level strain design approaches and mixed-integer programming solution techniques. PLoS ONE 6:e24162.10.1371/journal.pone.0024162
31. Kochanowski K. Sauer U. Chubukov V. (2013). Somewhat in control – the role of transcription in regulating microbial metabolic fluxes. Curr. Opin. Biotechnol. 24, 987–993.10.1016/j.copbio.2013.03.014
32. Lai S. Zhang Y. Liu S. Liang Y. Shang X. Chai X. et al. (2012). Metabolic engineering and flux analysis of Corynebacterium glutamicum for L-serine production. Sci. China Life Sci. 55, 283–290.10.1007/s11427-012-4304-0
33. Lee J. W. Na D. Park J. M. Lee J. Choi S. Lee S. Y. (2012). Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat. Chem. Biol. 8, 536–546.10.1038/nchembio.970
34. Lee K. H. Park J. H. Kim T. Y. Kim H. U. Lee S. Y. (2007). Systems metabolic engineering of Escherichia coli for L-threonine production. Mol. Syst. Biol. 3, 149.10.1038/msb4100196
35. Lee S. J. Lee D. Y. Kim T. Y. Kim B. H. Lee J. Lee S. Y. (2005). Metabolic engineering of Escherichia coli for enhanced production of succinic acid, based on genome comparison and in silico gene knockout simulation. Appl. Environ. Microbiol. 71, 7880–7887.10.1128/AEM.71.12.7880-7887.2005
36. Li M. Ho P. Y. Yao S. Shimizu K. (2006). Effect of sucA or sucC gene knockout on the metabolism in Escherichia coli based on gene expressions, enzyme activities, intracellular metabolite concentrations and metabolic fluxes by 13C-labeling experiments. Biochem. Eng. J. 30, 289–296.10.1016/j.bej.2006.05.011
37. Li Y. Chen G. K. Tong X. W. Zhang H. T. Liu X. G. Liu Y. H. et al. (2012). Construction of Escherichia coli strains producing L-serine from glucose. Biotechnol. Lett. 34, 1525–1530.10.1007/s10529-012-0937-0
38. Lin H. Bennett G. N. San K. Y. (2005a). Chemostat culture characterization of Escherichia coli mutant strains metabolically engineered for aerobic succinate production: a study of the modified metabolic network based on metabolite profile, enzyme activity, and gene expression profile. Metab. Eng. 7, 337–352.10.1016/j.ymben.2005.06.002
39. Lin H. Bennett G. N. San K. Y. (2005b). Fed-batch culture of a metabolically engineered Escherichia coli strain designed for high-level succinate production and yield under aerobic conditions. Biotechnol. Bioeng. 90, 775–779.10.1002/bit.20458
40. Litsanov B. Kabus A. Brocker M. Bott M. (2012). Efficient aerobic succinate production from glucose in minimal medium with Corynebacterium glutamicum. Microb. Biotechnol. 5, 116–128.10.1111/j.1751-7915.2011.00310.x
41. MacKintosh C. Nimmo H. G. (1988). Purification and regulatory properties of isocitrate lyase from Escherichia coli ML308. Biochem. J. 250, 25–31.
42. Mahadevan R. Edwards J. S. Doyle F. J. III (2002). Dynamic flux balance analysis of diauxic growth in Escherichia coli. Biophys. J. 83, 1331–1340.10.1016/S0006-3495(02)73903-9
43. Maia P. Vilaca P. Rocha I. Pont M. Tomb J. F. Rocha M. (2012). An integrated computational environment for elementary modes analysis of biochemical networks. Int. J. Data Min. Bioinform. 6, 382–395.10.1504/IJDMB.2012.049292
44. Millard C. S. Chao Y. P. Liao J. C. Donnelly M. I. (1996). Enhanced production of succinic acid by overexpression of phosphoenolpyruvate carboxylase in Escherichia coli. Appl. Environ. Microbiol. 62, 1808–1810.
45. Nikolaev E. V. (2010). The elucidation of metabolic pathways and their improvements using stable optimization of large-scale kinetic models of cellular systems. Metab. Eng. 12, 26–38.10.1016/j.ymben.2009.08.010
46. Ogawa T. Murakami K. Mori H. Ishii N. Tomita M. Yoshin M. (2007). Role of phosphoenolpyruvate in the NADP-isocitrate dehydrogenase and isocitrate lyase reaction in Escherichia coli. J. Bacteriol. 189, 1176–1178.10.1128/JB.01628-06
47. Osterhout R. E. Pharkya P. Burgard A. P. (2011). Microorganisms and methods for the production of ethylene glycol. US 13/086,295.
48. Partridge J. D. Sanguinetti G. Dibden D. P. Roberts R. E. Poole R. K. Green J. (2007). Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components. J. Biol. Chem. 282, 11230–11237.10.1074/jbc.M700728200
49. Partridge J. D. Scott C. Tang Y. Poole R. K. Green J. (2006). Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions. J. Biol. Chem. 281, 27806–27815.10.1074/jbc.M603450200
50. 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, 3171–3179.10.1128/JB.187.9.3171-3179.2005
51. Pharkya P. Burgard A. P. Maranas C. D. (2004). OptStrain: a computational framework for redesign of microbial production systems. Genome Res. 14, 2367–2376.10.1101/gr.2872004
52. Ranganathan S. Suthers P. F. Maranas C. D. (2010). OptForce: an optimization procedure for identifying all genetic manipulations leading to targeted overproductions. PLoS Comput. Biol. 6:e1000744.10.1371/journal.pcbi.1000744
53. Rocha I. Maia P. Evangelista P. Vilaca P. Soares S. Pinto J. P. et al. (2010). OptFlux: an open-source software platform for in silico metabolic engineering. BMC Syst. Biol. 4:45.10.1186/1752-0509-4-45
54. Sahinidis N. V. (1996). BARON: a general purpose global optimization software package. J. Global Optim. 8, 201–205.10.1007/BF00138693
55. Salmon K. Hung S. P. Mekjian K. Baldi P. Hatfield G. W. Gunsalus R. P. (2003). Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J. Biol. Chem. 278, 29837–29855.10.1074/jbc.M213060200
56. Salmon K. A. Hung S. P. Steffen N. R. Krupp R. Baldi P. Hatfield G. W. et al. (2005). Global gene expression profiling in Escherichia coli K12: effects of oxygen availability and ArcA. J. Biol. Chem. 280, 15084–15096.10.1074/jbc.M414030200
57. Sanchez A. M. Bennett G. N. San K. Y. (2005). Efficient succinic acid production from glucose through overexpression of pyruvate carboxylase in an Escherichia coli alcohol dehydrogenase and lactate dehydrogenase mutant. Biotechnol. Prog. 21, 358–365.10.1021/bp049676e
58. Sanwal B. D. Duckworth H. W. Hollier M. L. (1972). Regulation of phosphoglucomutase. Biochem. J. 128, 26–27.
59. Segre D. Vitkup D. Church G. M. (2002). Analysis of optimality in natural and perturbed metabolic networks. Proc. Natl. Acad. Sci. U.S.A. 99, 15112–15117.10.1073/pnas.232349399
60. Smallbone K. Simeonidis E. Swainston N. Mendes P. (2010). Towards a genome-scale kinetic model of cellular metabolism. BMC Syst. Biol. 4:6.10.1186/1752-0509-4-6
61. Song H. S. Ramkrishna D. (2012). Prediction of dynamic behavior of mutant strains from limited wild-type data. Metab. Eng. 14, 69–80.10.1016/j.ymben.2012.02.003
62. Sprenger G. A. Schorken U. Sprenger G. Sahm H. (1995). Transaldolase B of Escherichia coli K-12: cloning of its gene, talB, and characterization of the enzyme from recombinant strains. J. Bacteriol. 177, 5930–5936.
63. Tan Y. Liao J. C. (2012). Metabolic ensemble modeling for strain engineers. Biotechnol. J. 7, 343–353.10.1002/biot.201100186
64. Tan Y. Rivera J. G. Contador C. A. Asenjo J. A. Liao J. C. (2011). Reducing the allowable kinetic space by constructing ensemble of dynamic models with the same steady-state flux. Metab. Eng. 13, 60–75.10.1016/j.ymben.2010.11.001
65. Tepper N. Shlomi T. (2010). Predicting metabolic engineering knockout strategies for chemical production: accounting for competing pathways. Bioinformatics 26, 536–543.10.1093/bioinformatics/btp704
66. Tran L. M. Rizk M. L. Liao J. C. (2008). Ensemble modeling of metabolic networks. Biophys. J. 95, 5606–5617.10.1529/biophysj.108.135442
67. Villaverde F. A. Henriques D. Smallbone K. Bongard S. Schmid J. Cicin-Sain D. et al. (2014). BioPreDyn-bench: benchmark problems for kinetic modelling in systems biology. BioPreDyn-Bench arXiv:1407.5856.
68. Wang Q. Qi Y. Yin N. Lai L. (2014). Discovery of novel allosteric effectors based on the predicted allosteric sites for Escherichia coli D-3-phosphoglycerate dehydrogenase. PLoS ONE 9:e94829.10.1371/journal.pone.0094829
69. Wu H. Li Z. M. Zhou L. Ye Q. (2007). Improved succinic acid production in the anaerobic culture of an Escherichia coli pflB ldhA double mutant as a result of enhanced anaplerotic activities in the preceding aerobic culture. Appl. Environ. Microbiol. 73, 7837–7843.10.1128/AEM.01546-07
70. Xu P. Ranganathan S. Fowler Z. L. Maranas C. D. Koffas M. A. (2011). Genome-scale metabolic network modeling results in minimal interventions that cooperatively force carbon flux towards malonyl-CoA. Metab. Eng. 13, 578–587.10.1016/j.ymben.2011.06.008
71. Zhang X. Jantama K. Moore J. C. Jarboe L. R. Shanmugam K. T. Ingram L. O. (2009). Metabolic evolution of energy-conserving pathways for succinate production in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 106, 20180–20185.10.1073/pnas.0905396106
72. Zhu N. Xia H. Wang Z. Zhao X. Chen T. (2013). Engineering of acetate recycling and citrate synthase to improve aerobic succinate production in Corynebacterium glutamicum. PLoS ONE 8:e60659.10.1371/journal.pone.0060659
73. Zomorrodi A. R. Suthers P. F. Ranganathan S. Maranas C. D. (2012). Mathematical optimization applications in metabolic networks. Metab. Eng. 14, 672–686.10.1016/j.ymben.2012.09.005