Development and application of a differential method for reliable metabolome analysis in Escherichia coli

Analytical Biochemistry

Volumn 386, Issue 1, 2009, Pages 9-19

  Taymaz Nikerel, Hilal ^a   de Mey, Marjan ^b   Ras, Cor ^a   ten Pierick, Angela ^a   Seifar, Reza M ^a   van Dam, Jan C ^a   Heijnen, Joseph J ^a   van Gulik, Walter M ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b Faculty of Bioscience Engineering   (Belgium)

Author keywords

Escherichia coli; Metabolomics; Quantification of intracellular metabolites; Quenching; Rapid sampling

Indexed keywords

BIOMOLECULES; ESCHERICHIA COLI; IONIC STRENGTH; QUENCHING;

DEVELOPMENT AND APPLICATIONS; DIFFERENTIAL METHODS; ESCHERICHIA COLI K-12; EXTRACELLULAR METABOLITES; INTRACELLULAR METABOLITES; METABOLOME ANALYSIS; METABOLOMICS; RAPID SAMPLING;

METABOLITES;

AMINO ACID; METHANOL;

ANALYTIC METHOD; AQUEOUS SOLUTION; ARTICLE; BACTERIAL CELL; BACTERIUM CULTURE; ESCHERICHIA COLI; EXTRACELLULAR SPACE; INTERCELLULAR SPACE; IONIC STRENGTH; METABOLITE; METABOLOME; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; TURNOVER TIME;

ESCHERICHIA COLI;

EID: 58349085312     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2008.11.018     Document Type: Article

References (56)

1. Theobald U., Mailinger W., Baltes M., Rizzi M., and Reuss M. In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: I. Experimental observations. Biotechnol. Bioeng. 55 (1997) 305-316
2. Chassagnole C., Noisommit-Rizzi N., Schmid J.W., Mauch K., and Reuss M. Dynamic modeling of central carbon metabolism of Escherichia coli. Biotechnol. Bioeng. 79 (2002) 53-73
3. Visser D., van Zuylen G.A., van Dam J.C., Oudshoorn A., Eman M.R., Ras C., van Gulik W.M., Frank J., van Dedem G.W., and Heijnen J.J. Rapid sampling for analysis of in vivo kinetics using the BioScope: a system for continuous-pulse experiments. Biotechnol. Bioeng. 79 (2002) 674-681
4. Wu L., van Dam J., Schipper D., Kresnowati M.T., Proell A.M., Ras C., van Winden W.A., van Gulik W.M., and Heijnen J.J. Short-term metabolome dynamics and carbon, electron, and ATP balances in chemostat-grown Saccharomyces cerevisiae CEN.PK 113-7D following a glucose pulse. Appl. Environ. Microbiol. 72 (2006) 3566-3577
5. Lowry O.H., Carter J., Ward J.B., and Glaser L. The effect of carbon and nitrogen sources on the level of metabolic intermediates in Escherichia coli. J. Biol. Chem. 246 (1971) 6511-6521
6. Tweeddale H., Notley-McRobb L., and Ferenci T. Effect of slow growth on metabolism of Escherichia coli, as revealed by global metabolite pool ("metabolome") analysis. J. Bacteriol. 180 (1998) 5109-5116
7. Liu X., Ng C., and Ferenci T. Global adaptations resulting from high population densities in Escherichia coli cultures. J. Bacteriol. 182 (2000) 4158-4164
8. Theobald U., Mailinger W., Reuss M., and Rizzi M. In vivo analysis of glucose-induced fast changes in yeast adenine nucleotide pool applying a rapid sampling technique. Anal. Biochem. 214 (1993) 31-37
9. Lange H.C., Eman M., van Zuijlen G., Visser D., van Dam J.C., Frank J., Teixeira de Mattos M.J., and Heijnen J.J. Improved rapid sampling for in vivo kinetics of intracellular metabolites in Saccharomyces cerevisiae. Biotechnol. Bioeng. 75 (2001) 406-415
10. Schaefer U., Boos W., Takors R., and Weuster-Botz D. Automated sampling device for monitoring intracellular metabolite dynamics. Anal. Biochem. 270 (1999) 88-96
11. Buziol S., Bashir I., Baumeister A., Claaßen W., Noisommit-Rizzi N., Mailinger W., and Reuss M. New bioreactor-coupled rapid stopped-flow sampling technique for measurements of metabolite dynamics on a subsecond time scale. Biotechnol. Bioeng. 80 (2002) 632-636
12. Schaub J., Schiesling C., Reuss M., and Dauner M. Integrated sampling procedure for metabolome analysis. Biotechnol. Prog. 22 (2006) 1434-1442
13. de Koning W., and van Dam K. A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH. Anal. Biochem. 204 (1992) 118-123
14. 13C-labeling experiments together with measurements of enzyme activities and intracellular metabolite concentrations. Appl. Microbiol. Biotechnol. 63 (2004) 407-417
15. 13C-labelling experiments together with enzyme activity assays and intracellular metabolite measurements. FEMS Microbiol. Lett. 235 (2004) 17-23
16. 3 under those limiting continuous cultures. Biochem. Eng. J. 26 (2005) 38-49
17. Bolten C.J., Kiefer P., Letisse F., Portais J.C., and Wittmann C. Sampling for metabolome analysis of microorganisms. Anal. Chem. 79 (2007) 3843-3849
18. Wittmann C., Kromer J.O., Kiefer P., Binz T., and Heinzle E. Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria. Anal. Biochem. 327 (2004) 135-139
19. Villas-Boas S.G., Hojer-Pedersen J., Akesson M., Smedsgaard J., and Nielsen J. Global metabolite analysis of yeast: evaluation of sample preparation methods. Yeast 22 (2005) 1155-1169
20. Villas-Boas S.G., and Bruheim P. Cold glycerol-saline: the promising quenching solution for accurate intracellular metabolite analysis of microbial cells. Anal. Biochem. 370 (2007) 87-97
21. Brauer M.J., Yuan J., Bennett B.D., Lu W., Kimball E., Botstein D., and Rabinowitz J.D. Conservation of the metabolomic response to starvation across two divergent microbes. Proc. Natl. Acad. Sci. USA 103 (2006) 19302-19307
22. Buchholz A., Takors R., and Wandrey C. Quantification of intracellular metabolites in Escherichia coli K12 using liquid chromatographic-electrospray ionization tandem mass spectrometric techniques. Anal. Biochem. 295 (2001) 129-137
23. Buchholz A., Hurlebaus J., Wandrey C., and Takors R. Metabolomics: quantification of intracellular metabolite dynamics. Biomol. Eng. 19 (2002) 5-15
24. Maharjan R.P., and Ferenci T. Global metabolite analysis: the influence of extraction methodology on metabolome profiles of Escherichia coli. Anal. Biochem. 313 (2003) 145-154
25. Rabinowitz J.D., and Kimball E. Acid acetonitrile for cellular metabolome extraction from Escherichia coli. Anal. Chem. 79 (2007) 6167-6173
26. Hiller J., Franco-Lara E., and Weuster-Botz D. Metabolic profiling of Escherichia coli cultivations: evaluation of extraction and metabolite analysis procedures. Biotechnol. Lett. 29 (2007) 1169-1178
27. Kimball E., and Rabinowitz J.D. Identifying decomposition products in extracts of cellular metabolites. Anal. Biochem. 358 (2006) 273-280
28. van Dam J.C., Eman M.R., Frank J., Lange H.C., van Dedem G.W.K., and Heijnen J.J. Analysis of glycolytic intermediates in Saccharomyces cerevisiae using anion exchange chromatography and electrospray ionization with tandem mass spectrometric detection. Anal. Chim. Acta 460 (2002) 209-218
29. Luo B., Groenke K., Takors R., Wandrey C., and Oldiges M. Simultaneous determination of multiple intracellular metabolites in glycolysis, pentose phosphate pathway, and tricarboxylic acid cycle by liquid chromatography-mass spectrometry. J. Chromatogr. A 1147 (2007) 153-164
30. Mashego M.R., Wu L., van Dam J.C., Ras C., Vinke J.L., van Winden W.A., van Gulik W.M., and Heijnen J.J. MIRACLE: mass isotopomer ratio analysis of U-13C-labeled extracts: a new method for accurate quantification of changes in concentrations of intracellular metabolites. Biotechnol. Bioeng. 85 (2004) 620-628
31. Wu L., Mashego M.R., van Dam J.C., Proell A.M., Vinke J.L., Ras C., van Winden W.A., van Gulik W.M., and Heijnen J.J. Quantitative analysis of the microbial metabolomics by isotope dilution mass spectrometry using uniformly 13C-labeled cell extracts as internal standards. Anal. Biochem. 336 (2005) 164-171
32. Verduyn C., Postma E., Scheffers W.A., and Vandijken J.P. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8 (1992) 501-517
33. Mashego M.R., van Gulik W.M., Vinke J.L., and Heijnen J.J. Critical evaluation of sampling techniques for residual glucose determination in carbon-limited chemostat culture of Saccharomyces cerevisiae. Biotechnol. Bioeng. 83 (2003) 395-399
34. Gonzalez B., Francois J., and Renaud M. A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Yeast 13 (1997) 1347-1356
35. R.M. Seifar, C. Ras, J.C. van Dam, W.M. van Gulik, J.J. Heijnen, W.A. van Winden, Quantitative analysis of intracellular nucleotides using ion pair reversed phase liquid chromatography-electrospray isotope dilution tandem mass spectrometry, Anal. Biochem., accepted for publication.
36. Pramanik J., and Keasling J.D. Stoichiometric model of Escherichia coli metabolism: incorporation of growth rate dependent biomass composition and mechanistic energy requirements. Biotechnol. Bioeng. 56 (1997) 398-421
37. Nanchen A., Schicker A., and Sauer U. Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli. Appl. Environ. Microbiol. 72 (2006) 1164-1172
38. Roels J.A. Energetics and Kinetics in Biotechnology (1983), Elsevier, Amsterdam
39. Canelas A.B., Ras C., ten Pierick A., van Dam J.C., Heijnen J.J., and van Gulik W.M. Leakage-free rapid quenching technique for yeast metabolomics. Metabolomics. 4 (2008) 226-239
40. Schwöppe C., Winkler H.H., and Neuhaus H.E. Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC). J. Bacteriol. 184 (2002) 2108-2115
41. Schwöppe C., Winkler H.H., and Neuhaus H.E. Connection of transport and sensing by UhpC, the sensor for external glucose-6-phosphate in Escherichia coli. Eur. J. Biochem. 270 (2003) 1450-1457
42. Mashego M.R., Rumbold K., de Mey M., Vandamme E., Soetaert W., and Heijnen J.J. Microbial metabolomics: past, present, and future methodologies. Biotechnol. Lett. 29 (2007) 1-16
43. Bolten C.J., and Wittmann C. Appropriate rapid sampling for intracellular amino acid analysis in five phylogenetically different yeasts. Biotechnol. Lett. 30 (2008) 1993-2000
44. Kayser A., Weber J., Hecht V., and Rinas U. Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture: I. Growth rate-dependent metabolic efficiency at steady state. Microbiology 151 (2005) 693-706
45. Kümmel A., Panke S., and Heinemann M. Systematic assignment of thermodynamic constraints in metabolic network models. BMC Bioinformatics 23 (2006) 512
46. Chapman A.G., Fall L., and Atkinson D.E. Adenylate energy charge in Escherichia coli during growth and starvation. J. Bacteriol. 108 (1971) 1072-1086
47. Visser D., van der Heijden R.T.J.M., Mauch K., Reuss M., and Heijnen J.J. Tendency modeling: a new approach to obtain simplified kinetic models of metabolism applied to Saccharomyces cerevisiae. Metab. Eng. 2 (2000) 252-275
48. Canelas A.B., van Gulik W.M., and Heijnen J.J. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steady-state and highly dynamic conditions. Biotechnol. Bioeng. 100 (2008) 734-743
49. Seeholzer S.H. Phosphoglucose isomerase: a ketol isomerase with aldol C2-epimerase activity. Proc. Natl. Acad. Sci. USA 90 (1993) 1237-1241
50. Grisolia S., and Carreras J. Phosphoglycerate mutase from yeast, chicken breast muscle, and kidney (2,3-PGA-dependent). Methods Enzymol. 42 (1975) 435-450
51. Wold F., and Ballou C.E. Studies on the enzyme enolase: I. Equilibrium studies. J. Biol. Chem. 227 (1957) 301-312
52. eq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J. Biol. Chem. 254 (1979) 6528-6537
53. Keruchenko J.S., Keruchenko I.D., Gladilin K.L., Zaitsev V.N., and Chirgadze N.Y. Purification, characterization, and preliminary X-ray study of fumarase from Saccharomyces cerevisiae. Biochim. Biophys. Acta 1122 (1992) 85-92
54. Kiser R.C., and Niehaus W.G. Purification and kinetic characterization of mannitol-1-phosphate dehydrogenase from Aspergillus niger. Arch. Biochem. Biophys. 211 (1981) 613-621
55. Wilcock A.R., and Goldberg D.M. Kinetic determination of malate dehydrogenase activity eliminating problems due to spontaneous conversion of oxaloacetate to pyruvate. Biochem. Med. 6 (1972) 116-126
56. Kishore N., Tewari Y.B., and Goldberg R.N. An investigation of the equilibrium of the reaction {l-aspartate(aq) + 2-oxoglutarate(aq) = oxaloacetate(aq) + l-glutamate(aq)}. J. Chem. Thermodyn. 30 (1998) 1373-1384