Optimal cofactor swapping can increase the theoretical yield for chemical production in Escherichia coli and Saccharomyces cerevisiae

Metabolic Engineering

Volumn 24, Issue , 2014, Pages 117-128

  King, Zachary A ^a   Feist, Adam M ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Technical University of Denmark   (Denmark)

Author keywords

Cofactor balancing; Constraint based modeling; Escherichia coli; Metabolic engineering; MILP; Saccharomyces cerevisiae; Theoretical yield

Indexed keywords

AMINO ACIDS; ENZYMES; ESCHERICHIA COLI; INTEGER PROGRAMMING; METABOLIC ENGINEERING; METABOLISM; STYRENE;

COFACTOR SPECIFICITY; COFACTORS; CONSTRAINT-BASED MODELING; GENOME-SCALE METABOLIC MODELS; HETEROLOGOUS PRODUCTION; MILP; OPTIMIZATION PROCEDURES; THEORETICAL YIELD;

YEAST;

1,3 PROPANEDIOL; 3 HYDROXYBUTYRIC ACID; 3 HYDROXYPROPANOATE; 3 HYDROXYVALERATE; ALCOHOL DEHYDROGENASE; ASPARTIC ACID; CARBON; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; ISOLEUCINE; LYSINE; OXIDOREDUCTASE; PROLINE; PUTRESCINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SERINE; STYRENE; UNCLASSIFIED DRUG; XYLOSE; 1,3-PROPANEDIOL; AMINO ACID; BETA-HYDROXYVALERIC ACID; ESCHERICHIA COLI PROTEIN; HYDRACRYLIC ACID; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROPANEDIOL DERIVATIVE; SACCHAROMYCES CEREVISIAE PROTEIN; VALERIC ACID DERIVATIVE;

ANAEROBIC GROWTH; ARTICLE; BIOMASS PRODUCTION; CHEMICAL ANALYSIS; CHEMICAL PARAMETERS; ENZYME MODIFICATION; ESCHERICHIA COLI; GENOME; GLUCOSE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; REACTION OPTIMIZATION; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; YEAST; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; GENETICS; METABOLISM;

3-HYDROXYBUTYRIC ACID; AMINO ACIDS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LACTIC ACID; NAD; NADP; OXIDOREDUCTASES; PENTANOIC ACIDS; PROPYLENE GLYCOLS; PUTRESCINE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STYRENE;

EID: 84901623994     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2014.05.009     Document Type: Article

References (57)

1. Adkins J., Pugh S., McKenna R., Nielsen D.R. Engineering microbial chemical factories to produce renewable "biomonomers". Front. Microbiol. 2012, 3:313. 10.3389/fmicb.2012.00313.
2. Becker J., Wittmann C. Systems and synthetic metabolic engineering for amino acid production - the heartbeat of industrial strain development. Curr. Opin. Biotechnol. 2012, 23:718-726. 10.1016/j.copbio.2011.12.025.
3. Becker S.A., Feist A.M., Mo M.L., Hannum G., Palsson B.Ø., Herrgård M.J. Quantitative prediction of cellular metabolism with constraint-based models. the COBRA Toolbox. Nat. Protoc. 2007, 2:727-738. 10.1038/nprot.2007.99.
4. Bengtsson O., Hahn-Hägerdal B., Gorwa-Grauslund M.F. Xylose reductase from Pichia stipitis with altered coenzyme preference improves ethanolic xylose fermentation by recombinant Saccharomyces cerevisiae. Biotechnol. Biofuels 2009, 2:9. 10.1186/1754-6834-2-9.
5. +-dependent formate dehydrogenase. Metab. Eng. 2002, 4:217-229. 10.1006/mben.2002.0227.
6. Berríos-Rivera S.J., Bennett G.N., San K.Y. The effect of increasing NADH availability on the redistribution of metabolic fluxes in Escherichia coli chemostat cultures. Metab. Eng. 2002, 4:230-237. 10.1006/mben.2002.0228.
7. + ratio, and the distribution of metabolites in Escherichia coli. Metab. Eng. 2002, 4:238-247. 10.1006/mben.2002.0229.
8. Berríos-Rivera S.J., Sánchez a.M., Bennett G.N., San K.Y. Effect of different levels of NADH availability on metabolite distribution in Escherichia coli fermentation in minimal and complex media. Appl. Microbiol. Biotechnol. 2004, 65:426-432. 10.1007/s00253-004-1609-3.
9. Bettiga M., Hahn-Hägerdal B., Gorwa-Grauslund M.F. Comparing the xylose reductase/xylitol dehydrogenase and xylose isomerase pathways in arabinose and xylose fermenting Saccharomyces cerevisiae strains. Biotechnol. Biofuels 2008, 1:16. 10.1186/1754-6834-1-16.
10. Blaschkowski H., Neuer G., Ludwig-Festl M., Knappe J. Routes of flavodoxin and ferredoxin reduction in Escherichia coli. Eur. J. Biochem. 1982, 123:563-569. 10.1111/j.1432-1033.1982.tb06569.x.
11. Chin J.W., Khankal R., Monroe C.A., Maranas C.D., Cirino P.C. Analysis of NADPH supply during xylitol production by engineered Escherichia coli. Biotechnol. Bioeng. 2009, 102:209-220. 10.1002/bit.22060.
12. Chung B.K.S., Lakshmanan M., Klement M., Mohanty B., Lee D.Y. Genome-scale in silico modeling and analysis for designing synthetic terpenoid-producing microbial cell factories. Chem. Eng. Sci. 2013, 103:100-108. 10.1016/j.ces.2012.09.006.
13. Covert M.W., Knight E.M., Reed J.L., Herrgård M.J., Palsson B.Ø. Integrating high-throughput and computational data elucidates bacterial networks. Nature 2004, 429:92-96. 10.1038/nature02456.
14. Feist A.M., Henry C.S., Reed J.L., Krummenacker M., Joyce A.R., Karp P.D., Broadbelt L.J., Hatzimanikatis V., Palsson B.Ø. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 2007, 3:121. 10.1038/msb4100155.
15. Feist A.M., Zielinski D.C., Orth J.D., Schellenberger J., Herrgård M.J., Palsson B.Ø. Model-driven evaluation of the production potential for growth-coupled products of Escherichia coli. Metab. Eng. 2010, 12:173-186. 10.1016/j.ymben.2009.10.003.
16. Ghosh A., Zhao H., Price N.D. Genome-scale consequences of cofactor balancing in engineered pentose utilization pathways in Saccharomyces cerevisiae. PLoS One 2011, 6:e27316. 10.1371/journal.pone.0027316.
17. Gottschalk G. Bacterial Metabolism 1986, Springer-Verlag, New York, NY. 2nd ed.
18. Hyung Lim J., Woo Seo S., Yeon Kim S., Yeol Jung G. Model-driven rebalancing of the intracellular redox state for optimization of a heterologous n-butanol pathway in Escherichia coli. Metab. Eng. 2013, 20:56-62. 10.1016/j.ymben.2013.09.003.
19. Jan J., Martinez I., Wang Y., Bennett G.N., San K.Y. Metabolic engineering and transhydrogenase effects on NADPH availability in Escherichia coli. Biotechnol. Prog. 2013, 29:1124-1130. 10.1002/btpr.1765.
20. Jang Y.S., Kim B., Shin J.H., Choi Y.J., Choi S., Song C.W., Lee J., Park H.G., Lee S.Y. Bio-based production of C2-C6 platform chemicals. Biotechnol. Bioeng. 2012, 109:2437-2459. 10.1002/bit.24599.
21. Kauffman K.J., Prakash P., Edwards J.S. Advances in flux balance analysis. Curr. Opin. Biotechnol. 2003, 14:491-496. 10.1016/j.copbio.2003.08.001.
22. King Z.A., Feist A.M. Optimizing cofactor specificity of oxidoreductase enzymes for the generation of microbial production strains-OptSwap. Ind. Biotechnol. 2013, 9:236-246. 10.1089/ind.2013.0005.
23. Lakshmanan M., Chung B.K.S., Liu C., Kim S.W., Lee D.Y. Cofactor modificiation analysis. a computational framework to identify cofactor specificity engineering targets for strain improvement. J. Bioinform. Biotechnol. 2013, 11:1343006.
24. Lee W.H., Kim M.D., Jin Y.S., Seo J.H. Engineering of NADPH regenerators in Escherichia coli for enhanced biotransformation. Appl. Microbiol. Biotechnol. 2013, 97:2761-2772. 10.1007/s00253-013-4750-z.
25. Lewis N.E., Hixson K.K., Conrad T.M., Lerman J.A., Charusanti P., Polpitiya A.D., Adkins J.N., Schramm G., Purvine S.O., Lopez-Ferrer D., Weitz K.K., Eils R., König R., Smith R.D., Palsson B.Ø. Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models. Mol. Syst. Biol. 2010, 6:390. 10.1038/msb.2010.47.
26. Lin H., Bennett G.N., San K.Y. Metabolic engineering of aerobic succinate production systems in Escherichia coli to improve process productivity and achieve the maximum theoretical succinate yield. Metab. Eng. 2005, 7:116-127. 10.1016/j.ymben.2004.10.003.
27. Londesborough, J., Penttilae, M., Richard, P., Verho, R., 2003. Fungal micro-organism having an increased ability to carry out biotechnological process(es). WO 2003/038067 A1.
28. Lunzer M., Miller S.P., Felsheim R., Dean A.M. The biochemical architecture of an ancient adaptive landscape. Science 2005, 310:499-501. 10.1126/science.1115649.
29. Martínez I., Zhu J., Lin H., Bennett G.N., San K.Y. Replacing Escherichia coli NAD-dependent glyceraldehyde 3-phosphate dehydrogenase (GAPDH) with a NADP-dependent enzyme from Clostridium acetobutylicum facilitates NADPH dependent pathways. Metab. Eng. 2008, 10:352-359. 10.1016/j.ymben.2008.09.001.
30. McKenna R., Nielsen D.R. Styrene biosynthesis from glucose by engineered E. coli. Metab. Eng. 2011, 13:544-554. 10.1016/j.ymben.2011.06.005.
31. Mo M.L., Palsson B.Ø., Herrgård M.J. Connecting extracellular metabolomic measurements to intracellular flux states in yeast. BMC Syst. Biol. 2009, 3:37. 10.1186/1752-0509-3-37.
32. Murarka A., Dharmadi Y., Yazdani S.S., Gonzalez R. Fermentative utilization of glycerol by Escherichia coli and its implications for the production of fuels and chemicals. Appl. Environ. Microbiol. 2008, 74:1124-1135. 10.1128/AEM.02192-07.
33. Nissen T.L., Anderlund M., Nielsen J., Villadsen J., Kielland-Brandt M.C. Expression of a cytoplasmic transhydrogenase in Saccharomyces cerevisiae results in formation of 2-oxoglutarate due to depletion of the NADPH pool. Yeast 2001, 18:19-32. http://dx.doi.org/10.1002/1097-0061(200101)18:119::AID-YEA6503.0.CO;2-5.
34. Olavarría K., Valdés D., Cabrera R. The cofactor preference of glucose-6-phosphate dehydrogenase from Escherichia coli-modeling the physiological production of reduced cofactors. FEBS J. 2012, 279:2296-2309. 10.1111/j.1742-4658.2012.08610.x.
35. Orth J.D., Conrad T.M., Na J., Lerman J.A., Nam H., Feist A.M., Palsson B.Ø. A comprehensive genome-scale reconstruction of Escherichia coli metabolism-2011. Mol. Syst. Biol. 2011, 7:535. 10.1038/msb.2011.65.
36. Price N.D., Reed J.L., Palsson B.Ø. Genome-scale models of microbial cells. evaluating the consequences of constraints. Nat. Rev. Microbiol. 2004, 2:886-897. 10.1038/nrmicro1023.
37. Qi W.W., Vannelli T., Breinig S., Ben-Bassat A., Gatenby A.A., Haynie S.L., Sariaslani F.S. Functional expression of prokaryotic and eukaryotic genes in Escherichia coli for conversion of glucose to p-hydroxystyrene. Metab. Eng. 2007, 9:268-276. 10.1016/j.ymben.2007.01.002.
38. Qian Z.G., Xia X.X., Lee S.Y. Metabolic engineering of Escherichia coli for the production of putrescine. a four carbon diamine. Biotechnol. Bioeng. 2009, 104:651-662. 10.1002/bit.22502.
39. Rathnasingh C., Raj S.M., Jo J.E., Park S. Development and evaluation of efficient recombinant Escherichia coli strains for the production of 3-hydroxypropionic acid from glycerol. Biotechnol. Bioeng. 2009, 104:729-739. 10.1002/bit.22429.
40. Rathnasingh C., Raj S.M., Lee Y., Catherine C., Ashok S., Park S. Production of 3-hydroxypropionic acid via malonyl-CoA pathway using recombinant Escherichia coli strains. J. Biotechnol. 2012, 157:633-640. 10.1016/j.jbiotec.2011.06.008.
41. Russell J., Cook G. Energetics of bacterial growth. balance of anabolic and catabolic reactions. Microbiol. Mol. Biol. Rev. 1995, 59:48-62.
42. Sanchez A.M., Andrews J., Hussein I., Bennett G.N., San K.Y. Effect of overexpression of a soluble pyridine nucleotide transhydrogenase (UdhA) on the production of poly(3-hydroxybutyrate) in Escherichia coli. Biotechnol. Prog. 2006, 22:420-425. 10.1021/bp050375u.
43. Sauer U., Canonaco F., Heri S., Perrenoud A., Fischer E. The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J. Biol. Chem. 2004, 279:6613-6619. 10.1074/jbc.M311657200.
44. Shen C.R., Lan E.I., Dekishima Y., Baez A., Cho K.M., Liao J.C. Driving forces enable high-titer anaerobic 1-butanol synthesis in Escherichia coli. Appl. Environ. Microbiol. 2011, 77:2905-2915. 10.1128/AEM.03034-10.
45. +-dependent malic enzyme in an Escherichia coli mutant. Appl. Environ. Microbiol. 1997, 63:2695-2701.
46. Tang X., Tan Y., Zhu H., Zhao K., Shen W. Microbial conversion of glycerol to 1,3-propanediol by an engineered strain of Escherichia coli. Appl. Environ. Microbiol. 2009, 75:1628-1634. 10.1128/AEM.02376-08.
47. Trinh C.T. Elucidating and reprogramming Escherichia coli metabolisms for obligate anaerobic n-butanol and isobutanol production. Appl. Microbiol. Biotechnol. 2012, 95:1083-1094. 10.1007/s00253-012-4197-7.
48. Tseng H.C., Harwell C.L., Martin C.H., Prather K.L.J. Biosynthesis of chiral 3-hydroxyvalerate from single propionate-unrelated carbon sources in metabolically engineered E. coli. Microb. Cell Fact. 2010, 9:96. 10.1186/1475-2859-9-96.
49. Tseng H.C., Martin C.H., Nielsen D.R., Prather K.L.J. Metabolic engineering of Escherichia coli for enhanced production of (R)- and (S)-3-hydroxybutyrate. Appl. Environ. Microbiol. 2009, 75:3137-3145. 10.1128/AEM.02667-08.
50. Ui S., Takusagawa Y., Sato T., Ohtsuki T., Mimura A., Ohkuma M., Kudo T. Production of L-2,3-butanediol by a new pathway constructed in Escherichia coli. Lett. Appl. Microbiol. 2004, 39:533-537. 10.1111/j.1472-765X.2004.01622.x.
51. Verho R., Londesborough J., Penttilä M., Richard P. Engineering redox cofactor regeneration for improved pentose fermentation in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2003, 69:5892. 10.1128/AEM.69.10.5892.
52. Villadsen, J., Nielsen, J., Lidén, G., 2011. Chemicals from metabolic pathways. In: Bioreaction Engineering Principles. Springer, Boston, MA, USA, pp. 7-62 (Chapter 2). http://dx.doi.org/10.1007/978-1-4419-9688-6.
53. Wang B., Wang P., Zheng E., Chen X., Zhao H., Song P., Su R., Li X., Zhu G. Biochemical properties and physiological roles of NADP-dependent malic enzyme in Escherichia coli. J. Microbiol. 2011, 49:797-802. 10.1007/s12275-011-0487-5.
54. Yan Y., Lee C.C., Liao J.C. Enantioselective synthesis of pure (R,R)-2,3-butanediol in Escherichia coli with stereospecific secondary alcohol dehydrogenases. Org. Biomol. Chem. 2009, 7:3914-3917. 10.1039/b913501d.
55. Yim H., Haselbeck R., Niu W., Pujol-Baxley C., Burgard A., Boldt J., Khandurina J., Trawick J.D., Osterhout R.E., Stephen R., Estadilla J., Teisan S., Schreyer H.B., Andrae S., Yang T.H., Lee S.Y., Burk M.J., Van Dien S. Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat. Chem. Biol. 2011, 7:445-452. 10.1038/nchembio.580.
56. Zhang X., Jantama K., Moore J.C., Shanmugam K.T., Ingram L.O. Production of L -alanine by metabolically engineered Escherichia coli. Appl. Microbiol. Biotechnol. 2007, 77:355-366. 10.1007/s00253-007-1170-y.
57. Zhu G., Golding G.B., Dean A.M. The selective cause of an ancient adaptation. Science 2005, 307:1279-1282. 10.1126/science.1106974.