Carbon‐flux distribution in the central metabolic pathways of Corynebacterium glutamicum during growth on fructose

Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO2 during growth on...

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Published in:European Journal of Biochemistry Vol. 254; no. 1; pp. 96 - 102
Main Authors: Dominguez, Hélène, Rollin, Catherine, Guyonvarch, Armel, Guerquin‐Kern, Jean‐Luc, Cocaign‐Bousquet, Muriel, Lindley, Nicholas D.
Format: Journal Article
Language:English
Published: Berlin & Heidelberg Springer‐Verlag 15-05-1998
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Abstract Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO2 during growth on fructose. These differences in carbon‐metabolite accumulation are indicative of a different pattern of carbon‐flux distribution through the central metabolic pathways. Growth on glucose has been previously shown to involve a high flux (> 50 % of total glucose consumption) via the pentose pathway to generate anabolic reducing equivalents. NMR analysis of carbon‐isotope distribution patterns of the glutamate pool after growth on 1‐13C‐ or 6‐13C‐enriched fructose indicates that the contribution of the pentose pathway is significantly diminished during exponential growth on fructose with glycolysis being the predominant pathway (80 % of total fructose consumption). The increased flux through glycolysis during growth on fructose is associated with an increased NADH/NAD+ ratio susceptible to inhibit both glyceraldehyde‐3‐phosphate dehydrogenase and pyruvate dehydrogenase, and provoking the overflow of metabolites derived from the substrates of these two enzymes. The biomass yield observed experimentally is higher than can be estimated from the apparent quantity of NADPH associated with the pentose pathway and the flux through isocitrate dehydrogenase, suggesting an additional reaction yielding NADPH. This may involve a modified tricarboxylic acid cycle involving malic enzyme, expressed to significantly higher levels during growth on fructose than on glucose, and a pyruvate carboxylating anaplerotic enzyme.
AbstractList Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO2 during growth on fructose. These differences in carbon-metabolite accumulation are indicative of a different pattern of carbon-flux distribution through the central metabolic pathways. Growth on glucose has been previously shown to involve a high flux (> 50% of total glucose consumption) via the pentose pathway to generate anabolic reducing equivalents. NMR analysis of carbon-isotope distribution patterns of the glutamate pool after growth on 1-13C- or 6-13C-enriched fructose indicates that the contribution of the pentose pathway is significantly diminished during exponential growth on fructose with glycolysis being the predominant pathway (80% of total fructose consumption). The increased flux through glycolysis during growth on fructose is associated with an increased NADH/NAD+ ratio susceptible to inhibit both glyceraldehyde-3-phosphate dehydrogenase and pyruvate dehydrogenase, and provoking the overflow of metabolites derived from the substrates of these two enzymes. The biomass yield observed experimentally is higher than can be estimated from the apparent quantity of NADPH associated with the pentose pathway and the flux through isocitrate dehydrogenase, suggesting an additional reaction yielding NADPH. This may involve a modified tricarboxylic acid cycle involving malic enzyme, expressed to significantly higher levels during growth on fructose than on glucose, and a pyruvate carboxylating anaplerotic enzyme.
Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO sub(2) during growth on fructose. These differences in carbon-metabolite accumulation are indicative of a different pattern of carbon-flux distribution through the central metabolic pathways. Growth on glucose has been previously shown to involve a high flux (> 50% of total glucose consumption) via the pentose pathway to generate anabolic reducing equivalents. NMR analysis of carbon-isotope distribution patterns of the glutamate pool after growth on 1- super(13)C- or 6- super(13)C-enriched fructose indicates that the contribution of the pentose pathway is significantly diminished during exponential growth on fructose with glycolysis being the predominant pathway (80% of total fructose consumption). The increased flux through glycolysis during growth on fructose is associated with an increased NADH/NAD super(+) ratio susceptible to inhibit both glyceraldehyde-3-phosphate dehydrogenase and pyruvate dehydrogenase, and provoking the overflow of metabolites derived from the substrates of these two enzymes. The biomass yield observed experimentally is higher than can be estimated from the apparent quantity of NADPH associated with the pentose pathway and the flux through isocitrate dehydrogenase, suggesting an additional reaction yielding NADPH. This may involve a modified tricarboxylic acid cycle involving malic enzyme, expressed to significantly higher levels during growth on fructose than on glucose, and a pyruvate carboxylating anaplerotic enzyme.
Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO 2 during growth on fructose. These differences in carbon‐metabolite accumulation are indicative of a different pattern of carbon‐flux distribution through the central metabolic pathways. Growth on glucose has been previously shown to involve a high flux (> 50 % of total glucose consumption) via the pentose pathway to generate anabolic reducing equivalents. NMR analysis of carbon‐isotope distribution patterns of the glutamate pool after growth on 1‐ 13 C‐ or 6‐ 13 C‐enriched fructose indicates that the contribution of the pentose pathway is significantly diminished during exponential growth on fructose with glycolysis being the predominant pathway (80 % of total fructose consumption). The increased flux through glycolysis during growth on fructose is associated with an increased NADH/NAD + ratio susceptible to inhibit both glyceraldehyde‐3‐phosphate dehydrogenase and pyruvate dehydrogenase, and provoking the overflow of metabolites derived from the substrates of these two enzymes. The biomass yield observed experimentally is higher than can be estimated from the apparent quantity of NADPH associated with the pentose pathway and the flux through isocitrate dehydrogenase, suggesting an additional reaction yielding NADPH. This may involve a modified tricarboxylic acid cycle involving malic enzyme, expressed to significantly higher levels during growth on fructose than on glucose, and a pyruvate carboxylating anaplerotic enzyme.
Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in part due to the production of overflow metabolites (dihydroxyacetone and lactate) but also to the increased production of CO2 during growth on fructose. These differences in carbon-metabolite accumulation are indicative of a different pattern of carbon-flux distribution through the central metabolic pathways. Growth on glucose has been previously shown to involve a high flux (> 50% of total glucose consumption) via the pentose pathway to generate anabolic reducing equivalents. NMR analysis of carbon-isotope distribution patterns of the glutamate pool after growth on 1-13C- or 6-13C-enriched fructose indicates that the contribution of the pentose pathway is significantly diminished during exponential growth on fructose with glycolysis being the predominant pathway (80% of total fructose consumption). The increased flux through glycolysis during growth on fructose is associated with an increased NADH/NAD+ ratio susceptible to inhibit both glyceraldehyde-3-phosphate dehydrogenase and pyruvate dehydrogenase, and provoking the overflow of metabolites derived from the substrates of these two enzymes. The biomass yield observed experimentally is higher than can be estimated from the apparent quantity of NADPH associated with the pentose pathway and the flux through isocitrate dehydrogenase, suggesting an additional reaction yielding NADPH. This may involve a modified tricarboxylic acid cycle involving malic enzyme, expressed to significantly higher levels during growth on fructose than on glucose, and a pyruvate carboxylating anaplerotic enzyme.
Author Lindley, Nicholas D.
Cocaign‐Bousquet, Muriel
Guerquin‐Kern, Jean‐Luc
Guyonvarch, Armel
Dominguez, Hélène
Rollin, Catherine
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  fullname: Cocaign‐Bousquet, Muriel
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  givenname: Nicholas D.
  surname: Lindley
  fullname: Lindley, Nicholas D.
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Keywords RAPPORT NADH NAD
Language English
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Notes 3‐phosphoglycerate kinase
EC5.3.1.1
Enzymes.
fructose‐diphosphatase
EC1.1.1.49
EC2.7.5.1
EC2.7.1.4
EC2.7.2.3
EC1.1.1.40
Abbreviation.
glucose‐6‐phosphate dehydrogenase
EC1.1.1.44
1‐phosphofructokinase
33 561 559 400.
PTS, phosphotransferase system of sugar uptake.
6‐phosphofructokinase
E‐mail
phosphoglucose isomerase
lindley@insa‐tlse.fr
EC2.7.1.56
EC2.7.1.11
6‐phosphogluconate dehydrogenase
EC1.2.1.12
triosephosphate isomerase
.
glyceraldehyde‐3‐phosphate dehydrogenase
Fructokinase
EC5.1.3.9
Correspondence to
malic enzyme
Fax
phosphoglucose mutase
EC3.1.3.11
N. D. Lindley, Dept. Génie Biochimique et Alimentaire, Institut National des Sciences Appliquées, Complexe Scientifique de Rangueil, F‐31077 Toulouse cedex 4, France
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Snippet Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in...
Growth of Corynebacterium glutamicum on fructose was significantly less than that obtained on glucose, despite similar rates of substrate uptake. This was in...
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SubjectTerms Biochemistry, Molecular Biology
Biological Transport - physiology
Carbon Radioisotopes - metabolism
Corynebacterium - growth & development
Corynebacterium - metabolism
Corynebacterium glutamicum
Fructose - metabolism
Glucose - metabolism
Glutamic Acid - metabolism
Glyceraldehyde-3-Phosphate Dehydrogenases - metabolism
Glycolysis - physiology
Life Sciences
Magnetic Resonance Spectroscopy
NAD - metabolism
NADH/NAD+ ratio
NADP - metabolism
NMR analysis
overflow metabolism
Pentose Phosphate Pathway - physiology
Phosphoenolpyruvate Sugar Phosphotransferase System - physiology
Title Carbon‐flux distribution in the central metabolic pathways of Corynebacterium glutamicum during growth on fructose
URI https://onlinelibrary.wiley.com/doi/abs/10.1046%2Fj.1432-1327.1998.2540096.x
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