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Journal of Bacteriology, July 2002, p. 3909-3916, Vol. 184, No. 14
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.14.3909-3916.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

The Glycolytic Flux in Escherichia coli Is Controlled by the Demand for ATP

Brian J. Koebmann,1 Hans V. Westerhoff,2,3 Jacky L. Snoep,4 Dan Nilsson,5 and Peter R. Jensen1*

Section of Molecular Microbiology, BioCentrum-DTU, Technical University of Denmark, DK-2800 Lyngby,1 CH Bio Ingredients, Chr. Hansen A/S, DK-2970 Hørsholm, Denmark,5 Departments of Molecular Cell Physiology,2 Mathematical Biochemistry, BioCentrum Amsterdam, Faculty of Biology, Free University, De Boelelaan 1087, NL-1081 HV Amsterdam, The Netherlands,3 Department of Biochemistry, University of Stellenbosch, 7602 Matieland, South Africa4

Received 4 March 2002/ Accepted 17 April 2002

The nature of the control of glycolytic flux is one of the central, as-yet-uncharacterized issues in cellular metabolism. We developed a molecular genetic tool that specifically induces ATP hydrolysis in living cells without interfering with other aspects of metabolism. Genes encoding the F1 part of the membrane-bound (F1F0) H+-ATP synthase were expressed in steadily growing Escherichia coli cells, which lowered the intracellular [ATP]/[ADP] ratio. This resulted in a strong stimulation of the specific glycolytic flux concomitant with a smaller decrease in the growth rate of the cells. By optimizing additional ATP hydrolysis, we increased the flux through glycolysis to 1.7 times that of the wild-type flux. The results demonstrate why attempts in the past to increase the glycolytic flux through overexpression of glycolytic enzymes have been unsuccessful: the majority of flux control (>75%) resides not inside but outside the pathway, i.e., with the enzymes that hydrolyze ATP. These data further allowed us to answer the question of whether catabolic or anabolic reactions control the growth of E. coli. We show that the majority of the control of growth rate resides in the anabolic reactions, i.e., the cells are mostly "carbon" limited. Ways to increase the efficiency and productivity of industrial fermentation processes are discussed.

* Corresponding author. Mailing address: Section of Molecular Microbiology, BioCentrum-DTU, Technical University of Denmark, Building 301, DK-2800 Kgs. Lyngby, Denmark. Phone: 45-45252510. Fax: 45-45932809. E-mail: prj{at}biocentrum.dtu.dk.

Journal of Bacteriology, July 2002, p. 3909-3916, Vol. 184, No. 14
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.14.3909-3916.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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