Comprehensive analysis of glucose and xylose metabolism in Escherichia coli under aerobic and anaerobic conditions by 13C metabolic flux analysis

Metabolic Engineering

Volumn 39, Issue , 2017, Pages 9-18

  Gonzalez, Jacqueline E ^a   Long, Christopher P ^a   Antoniewicz, Maciek R ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Co factor balances; Flux estimation; Metabolism; Model validation; Parallel labeling experiments

Indexed keywords

BIOMASS; CARBON DIOXIDE; CYTOLOGY; ECOLOGY; ESCHERICHIA COLI; GLUCOSE; METABOLISM; PHYSIOLOGY;

AEROBIC AND ANAEROBIC CONDITIONS; BIOMASS COMPOSITIONS; CO FACTORS; COMPREHENSIVE ANALYSIS; FLUX ESTIMATION; LIGNOCELLULOSIC BIOMASS; METABOLIC FLUX ANALYSIS; MODEL VALIDATION;

METABOLIC ENGINEERING;

ADENOSINE TRIPHOSPHATE; CARBON 13; FLAVINE ADENINE NUCLEOTIDE; GLUCOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; XYLOSE; CARBON; ESCHERICHIA COLI PROTEIN; OXYGEN;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOCHEMICAL COMPOSITION; BIOMASS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ESCHERICHIA COLI; FATTY ACID OXIDATION; GENE INACTIVATION; GLUCOSE METABOLISM; ISOTOPE LABELING; MACROMOLECULE; MICROBIAL BIOMASS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TURNOVER TIME; BIOLOGICAL MODEL; CARBON NUCLEAR MAGNETIC RESONANCE; LIPID METABOLISM; METABOLIC FLUX ANALYSIS; METABOLISM; PHYSIOLOGY; PROCEDURES;

AEROBIOSIS; ANAEROBIOSIS; CARBON ISOTOPES; CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUCOSE; LIPID METABOLISM; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; OXYGEN; XYLOSE;

EID: 84995622089     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2016.11.003     Document Type: Article

References (52)

1. Antoniewicz, M.R., 13C metabolic flux analysis: optimal design of isotopic labeling experiments. Curr. Opin. Biotechnol. 24 (2013), 1116–1121.
2. Antoniewicz, M.R., Methods and advances in metabolic flux analysis: a mini-review. J. Ind. Microbiol. Biotechnol. 42 (2015), 317–325.
3. Antoniewicz, M.R., Parallel labeling experiments for pathway elucidation and 13C metabolic flux analysis. Curr. Opin. Biotechnol. 36 (2015), 91–97.
4. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements. Metab. Eng. 8 (2006), 324–337.
5. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Accurate assessment of amino acid mass isotopomer distributions for metabolic flux analysis. Anal. Chem. 79 (2007), 7554–7559.
6. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Elementary metabolite units (EMU): a novel framework for modeling isotopic distributions. Metab. Eng. 9 (2007), 68–86.
7. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Measuring deuterium enrichment of glucose hydrogen atoms by gas chromatography/mass spectrometry. Anal. Chem. 83 (2011), 3211–3216.
8. Antoniewicz, M.R., Kraynie, D.F., Laffend, L.A., Gonzalez-Lergier, J., Kelleher, J.K., Stephanopoulos, G., Metabolic flux analysis in a nonstationary system: fed-batch fermentation of a high yielding strain of E. coli producing 1,3-propanediol. Metab. Eng. 9 (2007), 277–292.
9. Antoniewicz, M.R., Stephanopoulos, G., Kelleher, J.K., Evaluation of regression models in metabolic physiology: predicting fluxes from isotopic data without knowledge of the pathway. Metabolomics 2 (2006), 41–52.
10. Au, J., Choi, J., Jones, S.W., Venkataramanan, K.P., Antoniewicz, M.R., Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for C metabolic flux analysis. Metab. Eng. 26 (2014), 23–33.
11. Becker, S.A., Feist, A.M., Mo, M.L., Hannum, G., Palsson, B.O., Herrgard, M.J., Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Nat. Protoc. 2 (2007), 727–738.
12. Burgard, A.P., Pharkya, P., Maranas, C.D., Optknock: a bilevel programming framework for identifying gene knockout strategies for microbial strain optimization. Biotechnol. Bioeng. 84 (2003), 647–657.
13. Campbell, J.W., Morgan-Kiss, R.M., Cronan, J.E. Jr., A new Escherichia coli metabolic competency: growth on fatty acids by a novel anaerobic beta-oxidation pathway. Mol. Microbiol. 47 (2003), 793–805.
14. Chen, X., Alonso, A.P., Allen, D.K., Reed, J.L., Shachar-Hill, Y., Synergy between (13)C-metabolic flux analysis and flux balance analysis for understanding metabolic adaptation to anaerobiosis in E. coli. Metab Eng. 13 (2011), 38–48.
15. Choi, S., Song, C.W., Shin, J.H., Lee, S.Y., Biorefineries for the production of top building block chemicals and their derivatives. Metab. Eng. 28 (2015), 223–239.
16. Choudhary, M.K., Yoon, J.M., Gonzalez, R., Shanks, J.V., Re-examination of metabolic fluxes in Escherichia coli during anaerobic fermentation of glucose using 13C labeling experiments and 2-dimensional Nuclear Magnetic Resonance (NMR) Spectroscopy. Biotechnol. Bioprocess Eng. 16 (2011), 419–437.
17. Cordova, L.T., Antoniewicz, M.R., (13)C metabolic flux analysis of the extremely thermophilic, fast growing, xylose-utilizing Geobacillus strain LC300. Metab. Eng. 33 (2016), 148–157.
18. Cordova, L.T., Lu, J., Cipolla, R.M., Sandoval, N.R., Long, C.P., Antoniewicz, M.R., Co-utilization of glucose and xylose by evolved Thermus thermophilus LC113 strain elucidated by C metabolic flux analysis and whole genome sequencing. Metab. Eng. 37 (2016), 63–71.
19. Crown, S.B., Ahn, W.S., Antoniewicz, M.R., Rational design of (1)(3)C-labeling experiments for metabolic flux analysis in mammalian cells. BMC Syst. Biol., 6, 2012, 43.
20. Crown, S.B., Antoniewicz, M.R., Selection of tracers for 13C-metabolic flux analysis using elementary metabolite units (EMU) basis vector methodology. Metab. Eng. 14 (2012), 150–161.
21. Crown, S.B., Antoniewicz, M.R., Publishing 13C metabolic flux analysis studies: a review and future perspectives. Metab. Eng. 20 (2013), 42–48.
22. Crown, S.B., Long, C.P., Antoniewicz, M.R., Integrated 13C-metabolic flux analysis of 14 parallel labeling experiments in Escherichia coli. Metab. Eng. 28 (2015), 151–158.
23. Crown, S.B., Long, C.P., Antoniewicz, M.R., Optimal tracers for parallel labeling experiments and 13C metabolic flux analysis: a new precision and synergy scoring system. Metab. Eng. 38 (2016), 10–18.
24. Crown, S.B., Marze, N., Antoniewicz, M.R., Catabolism of branched chain amino acids contributes significantly to synthesis of odd-chain and even-chain fatty acids in 3T3-L1 adipocytes. PLoS One, 10, 2015, e0145850.
25. Edwards, J.S., Ramakrishna, R., Palsson, B.O., Characterizing the metabolic phenotype: a phenotype phase plane analysis. Biotechnol. Bioeng. 77 (2002), 27–36.
26. Feng, X., Zhao, H., Investigating xylose metabolism in recombinant Saccharomyces cerevisiae via 13C metabolic flux analysis. Microb Cell Factories, 12, 2013, 114.
27. Fernandez, C.A., Des Rosiers, C., Previs, S.F., David, F., Brunengraber, H., Correction of 13C mass isotopomer distributions for natural stable isotope abundance. J. Mass Spectrom. 31 (1996), 255–262.
28. Girio, F.M., Fonseca, C., Carvalheiro, F., Duarte, L.C., Marques, S., Bogel-Lukasik, R., Hemicelluloses for fuel ethanol: a review. Bioresour. Technol. 101 (2010), 4775–4800.
29. Hasona, A., Kim, Y., Healy, F.G., Ingram, L.O., Shanmugam, K.T., Pyruvate formate lyase and acetate kinase are essential for anaerobic growth of Escherichia coli on xylose. J. Bacteriol. 186 (2004), 7593–7600.
30. Kim, J., Reed, J.L., RELATCH: relative optimality in metabolic networks explains robust metabolic and regulatory responses to perturbations. Genome Biol., 13, 2012, R78.
31. King, Z.A., Lloyd, C.J., Feist, A.M., Palsson, B.O., Next-generation genome-scale models for metabolic engineering. Curr. Opin. Biotechnol. 35C (2015), 23–29.
32. Leighty, R.W., Antoniewicz, M.R., Parallel labeling experiments with [U-13C]glucose validate E. coli metabolic network model for 13C metabolic flux analysis. Metab. Eng. 14 (2012), 533–541.
33. Leighty, R.W., Antoniewicz, M.R., COMPLETE-MFA: complementary parallel labeling experiments technique for metabolic flux analysis. Metab. Eng. 20 (2013), 49–55.
34. Liu, L., Zhang, L., Tang, W., Gu, Y., Hua, Q., Yang, S., Jiang, W., Yang, C., Phosphoketolase pathway for xylose catabolism in Clostridium acetobutylicum revealed by 13C metabolic flux analysis. J. Bacteriol. 194 (2012), 5413–5422.
35. Long, C.P., Antoniewicz, M.R., Metabolic flux analysis of Escherichia coli knockouts: lessons from the Keio collection and future outlook. Curr. Opin. Biotechnol. 28 (2014), 127–133.
36. Long, C.P., Antoniewicz, M.R., Quantifying biomass composition by gas chromatography/mass spectrometry. Anal. Chem. 86 (2014), 9423–9427.
37. Long, C.P., Au, J., Gonzalez, J.E., Antoniewicz, M.R., 13C metabolic flux analysis of microbial and mammalian systems is enhanced with GC-MS measurements of glycogen and RNA labeling. Metab. Eng. 38 (2016), 65–72.
38. Long, C.P., Gonzalez, J.E., Sandoval, N.R., Antoniewicz, M.R., Characterization of physiological responses to 22 gene knockouts in Escherichia coli central carbon metabolism. Metab. Eng. 37 (2016), 102–113.
39. McConnell, B.O., Antoniewicz, M.R., Measuring the composition and stable-isotope labeling of algal biomass carbohydrates via gas chromatography/mass spectrometry. Anal. Chem. 88 (2016), 4624–4628.
40. Neidhardt, F.C., Escherichia Coli and Salmonella Typhimurium. 1987, ASM Press, Washington, D.C.
41. Noguchi, Y., Nakai, Y., Shimba, N., Toyosaki, H., Kawahara, Y., Sugimoto, S., Suzuki, E., The energetic conversion competence of Escherichia coli during aerobic respiration studied by 31P NMR using a circulating fermentation system. J. Biochem. 136 (2004), 509–515.
42. Perrenoud, A., Sauer, U., Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. J. Bacteriol. 187 (2005), 3171–3179.
43. Sandberg, T.E., Long, C.P., Gonzalez, J.E., Feist, A.M., Antoniewicz, M.R., Palsson, B.O., Evolution of E. coli on [U-13C]glucose reveals a negligible isotopic influence on metabolism and physiology. PLoS One, 11, 2016, e0151130.
44. Schmidt, A., Kochanowski, K., Vedelaar, S., Ahrne, E., Volkmer, B., Callipo, L., Knoops, K., Bauer, M., Aebersold, R., Heinemann, M., The quantitative and condition-dependent Escherichia coli proteome. Nat. Biotechnol. 34 (2016), 104–110.
45. Segre, D., Vitkup, D., Church, G.M., Analysis of optimality in natural and perturbed metabolic networks. Proc. Natl. Acad. Sci. USA 99 (2002), 15112–15117.
46. Shlomi, T., Berkman, O., Ruppin, E., Regulatory on/off minimization of metabolic flux changes after genetic perturbations. Proc. Natl. Acad. Sci. USA 102 (2005), 7695–7700.
47. Tao, H., Gonzalez, R., Martinez, A., Rodriguez, M., Ingram, L.O., Preston, J.F., Shanmugam, K.T., Engineering a homo-ethanol pathway in Escherichia coli: increased glycolytic flux and levels of expression of glycolytic genes during xylose fermentation. J. Bacteriol. 183 (2001), 2979–2988.
48. Taymaz-Nikerel, H., Borujeni, A.E., Verheijen, P.J., Heijnen, J.J., van Gulik, W.M., Genome-derived minimal metabolic models for Escherichia coli MG1655 with estimated in vivo respiratory ATP stoichiometry. Biotechnol. Bioeng. 107 (2010), 369–381.
49. Toya, Y., Nakahigashi, K., Tomita, M., Shimizu, K., Metabolic regulation analysis of wild-type and arcA mutant Escherichia coli under nitrate conditions using different levels of omics data. Mol. BioSyst., 2012.
50. Wasylenko, T.M., Stephanopoulos, G., Metabolomic and (13)C-metabolic flux analysis of a xylose-consuming Saccharomyces cerevisiae strain expressing xylose isomerase. Biotechnol. Bioeng. 112 (2015), 470–483.
51. Woolston, B.M., Edgar, S., Stephanopoulos, G., Metabolic engineering: past and future. Annu. Rev. Chem. Biomol. Eng. 4 (2013), 259–288.
52. Yoo, H., Stephanopoulos, G., Kelleher, J.K., Quantifying carbon sources for de novo lipogenesis in wild-type and IRS-1 knockout brown adipocytes. J. Lipid Res. 45 (2004), 1324–1332.