Absolute quantitation of glycolytic intermediates reveals thermodynamic shifts in Saccharomyces cerevisiae strains lacking PFK1 or ZWF1 genes

Journal of Bioscience and Bioengineering

Volumn 120, Issue 3, 2015, Pages 280-286

  Nishino, Shunsuke ^a   Okahashi, Nobuyuki ^a   Matsuda, Fumio ^a   Shimizu, Hiroshi ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Absolute quantitation; Central carbon metabolism; Gibbs free energy change; Liquid chromatography mass spectrometry; Saccharomyces cerevisiae

Indexed keywords

CARBON; CHROMATOGRAPHY; FREE ENERGY; GIBBS FREE ENERGY; GLUCOSE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MIXTURES; PHYSIOLOGY; THERMODYNAMIC PROPERTIES; THERMODYNAMICS;

ABSOLUTE QUANTITATION; CENTRAL CARBON METABOLISMS; GIBBS FREE ENERGY CHANGES; GLYCOLYTIC INTERMEDIATE; LIQUID CHROMATOGRAPHY - MASS SPECTROMETRIES; PHOSPHOGLUCOSE ISOMERASE; SACCHAROMYCES CEREVISIAE STRAINS; THERMODYNAMIC STATE;

YEAST;

CARBON 13; FRUCTOSE 1,6 BISPHOSPHATE; FUNGAL ENZYME; GLUCOSE; GLUCOSE 6 PHOSPHATE ISOMERASE; ISOMERASE; RIBOSE 5 PHOSPHATE KETOISOMERASE; TRANSALDOLASE; TRANSKETOLASE; UNCLASSIFIED DRUG; FRUCTOSE BISPHOSPHATE; FRUCTOSE-1,6-DIPHOSPHATE; RIBOSEPHOSPHATE ISOMERASE;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; ENERGY METABOLISM; FUNGAL CELL; FUNGAL GENE; FUNGAL METABOLISM; FUNGAL STRAIN; FUNGUS GROWTH; GLYCOLYSIS; ISOTOPE LABELING; LIMIT OF QUANTITATION; METABOLIC REGULATION; METABOLITE; NONHUMAN; PFK1 GENE; SACCHAROMYCES CEREVISIAE; STANDARD; THERMODYNAMICS; ZWF1 GENE; GENETICS; METABOLISM;

SACCHAROMYCES CEREVISIAE;

ALDOSE-KETOSE ISOMERASES; FRUCTOSEDIPHOSPHATES; GENES, FUNGAL; GLUCOSE; GLUCOSE-6-PHOSPHATE ISOMERASE; GLYCOLYSIS; REFERENCE STANDARDS; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS; TRANSALDOLASE; TRANSKETOLASE;

EID: 84938285581     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2015.01.012     Document Type: Article

References (37)

1. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2008, 72:379-412.
2. Kondo A., Ishii J.Y., Harac K., Hasunuma T., Matsuda F. Development of microbial cell factories for bio-refinery through synthetic bioengineering. J. Biotechnol. 2013, 163:204-216.
3. Ciriacy M., Breitenbach I. Physiological effects of seven different blocks in glycolysis in Saccharomyces cerevisiae. J. Bacteriol. 1979, 139:152-160.
4. Teusink B., Passarge J., Reijenga C.A., Esgalhado E., van der Weijden C.C., Schepper M., Walsh M.C., Bakker B.M., van Dam K., Westerhoff H.V., Snoep J.L. Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur. J. Biochem. 2000, 267:5313-5329.
5. Luo B., Groenke K., Takors R., Wandrey C., 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 2007, 1147:153-164.
6. Kell D.B., Brown M., Davey H.M., Dunn W.B., Spasic I., Olive S. Metabolic footprinting and systems biology: the medium is the message. Nat. Rev. Microbiol. 2005, 3:557-565.
7. Buchholz A., Takors R., Wandrey C. Quantification of intracellular metabolites in Escherichia coli K12 using liquid chromatographic-electrospray ionization tandem mass spectrometric techniques. Anal. Biochem. 2001, 295:129-137.
8. van Dam J.C., Eman M.R., Frank J., Lange H.C., van Dedem G.W.K., Heijnen S.J. Analysis of glycolytic intermediates in Saccharomyces cerevisiae using anion exchange chromatography and electrospray ionization with tandem mass spectrometric detection. Anal. Chim. Acta 2002, 460:209-218.
9. Shirai T., Matsuda F., Okamoto M., Kondo A. Evaluation of control mechanisms for Saccharomyces cerevisiae central metabolic reactions using metabolome data of eight single-gene deletion mutants. Appl. Microbiol. Biotechnol. 2013, 97:3569-3577.
10. Brauer M.J., Yuan J., Bennett B.D., Lu W., Kimball E., Botstein D., Rabinowitz J.D. Conservation of the metabolomic response to starvation across two divergent microbes. Proc. Natl. Acad. Sci. USA 2006, 103:19302-19307.
11. Büscher J.M., Czernik D., Ewald J.C., Sauer U., Zamboni N. Cross-platform comparison of methods for quantitative metabolomics of primary metabolism. Anal. Chem. 2009, 15:2135-2143.
12. Annesley T.M. Ion suppression in mass spectrometry. Clin. Chem. 2003, 49:1041-1044.
13. Bennett B.D., Yuan J., Kimball E.H., Rabinowitz J.D. Absolute quantitation of intracellular metabolite concentrations by an isotope ratio-based approach. Nat. Protoc. 2008, 3:1299-1311.
14. 13C-labeled extracts. A new method for accurate quantification of changes in concentrations of intracellular metabolites. Biotechnol. Bioeng. 2004, 85:620-628.
15. Klimacek M., Krahulec S., Sauer U., Nidetzky B. Limitations in xylose-fermenting Saccharomyces cerevisiae, made evident through comprehensive metabolite profiling and thermodynamic analysis. Appl. Environ. Microbiol. 2010, 76:7566-7574.
16. Ewald J.C., Matta T., Zamboni N. The integrated response of primary metabolites to gene deletions and the environment. Mol. Biosyst. 2013, 9:440-446.
17. Bennett B.D., Kimball E.H., Gao M., Osterhout R., Van Dien S.J., Rabinowitz J.D. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Boil. 2009, 5:593-599.
18. Bolten J.C., Kiefer P., Letisse F., Portais J.C., Wittmann C. Sampling for metabolome analysis of microorganisms. Anal. Chem. 2007, 79:3843-3849.
19. Kawase N., Tsugawa H., Bamba T., Fukusaki E. Different-batch metabolome analysis of Saccharomyces cerevisiae based on gas chromatography/mass spectrometry. J. Biosci. Bioeng. 2014, 117:248-255.
20. Kato H., Izumi Y., Hasunuma T., Matsuda F., Kondo A. Widely targeted metabolic profiling analysis of yeast central metabolites. J. Biosci. Bioeng. 2012, 113:665-673.
21. Goldberg R.N., Tewari Y.B., Bhat T.N. Thermodynamics of enzyme-catalyzed reactions-a database for quantitative biochemistry. Bioinformatics 2004, 20:2874-2877.
22. Tewari Y.B., Steckler D.K., Goldberg R.N. Thermodynamics of isomerization reactions involving sugar phosphates. J. Biol. Chem. 1988, 263:3664-3669.
23. Meyerhof O., Junowicz-Kocholaty R. The equilibria of isomerase and aldolase, and the problem of the phosphorylation of glyceraldehyde phosphate. J. Biol. Chem. 1943, 149:71-92.
24. Casazza J.P., Veech R.L. The interdependence of glycolytic and pentose cycle intermediates in ad libitum fed rats. J. Biol. Chem. 1986, 261:690-698.
25. Wold F., Ballou C.E. Studies on the enzyme enolase. I. Equilibrium studies. J. Biol. Chem. 1957, 227:301-312.
26. Dempo Y., Ohta E., Nakayama Y., Bamba T., Fukusaki E. Molar-based targeted metabolic profiling of cyanobacterial strains with potential for biological production. Metabolites 2014, 4:499-516.
27. Arvanitidis A., Heinisch J.J. Studies on the function of yeast phosphofructokinase subunits by in vitro mutagenesis. J. Biol. Chem. 1994, 269:911-918.
28. Heinisch J. Construction and physiological characterization of mutants disrupted in the phosphofructokinase genes of Saccharomyces cerevisiae. Curr. Genet. 1986, 11:227-234.
29. Pearce A.K., Crimmins K., Groussac E., Hewlins M.J.E., Dickinson J.R., Francois J., Booth I.R., Brown A.J.P. Pyruvate kinase (Pyk1) levels influence both the rate and direction of carbon flux in yeast under fermentative conditions. Microbiology 2001, 147:391-401.
30. Nogae I., Johnston M. Isolation and characterization of the ZWF1 gene of Saccharomyces cerevisiae, encoding glucose-6-phosphate dehydrogenase. Gene 1990, 96:161-169.
31. Veech R.L., Raijman L., Dalziel K., Krebs H.A. Disequilibrium in the triose phosphate isomerase system in rat liver isomerase. Biochem. J. 1969, 115:837-842.
32. Grisolia S., Carreras J. Phosphoglycerate mutase from yeast, chicken breast muscle, and kidney (2,3-PGA-dependent). Methods Enzymol. 1975, 42:435-450.
33. Fonvielle M., Coinçon M., Daher R., Desbenoit N., Kosieradzka K., Barilone N., Gicquel B., Sygusch J., Jackson M., Therisod M. Synthesis and biochemical evaluation of selective inhibitors of class II fructose bisphosphate aldolases: towards new synthetic antibiotics. Chemistry 2008, 14:8521-8529.
34. Rizzi M., Baltes M., Theobald U., Reuss M. In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: II. Mathematical model. Biotechnol. Bioeng. 1997, 20:592-608.
35. Tsugawa H., Tsujimoto Y., Sugitate K., Sakui N., Nishiumi S., Bamba T., Fukusaki E. Highly sensitive and selective analysis of widely targeted metabolomics using gas chromatography/triple-quadrupole mass spectrometry. J. Biosci. Bioeng. 2014, 117:122-128.
36. Picotti P., Bodenmiller B., Mueller L.N., Domon B., Aebersold R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138:795-806.
37. 13C metabolic flux analysis. Microb. Cell Fact. 2012, 11:87.