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Journal of Bacteriology, September 2009, p. 5510-5517, Vol. 191, No. 17
0021-9193/09/$08.00+0     doi:10.1128/JB.00562-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Respiration of Escherichia coli Can Be Fully Uncoupled via the Nonelectrogenic Terminal Cytochrome bd-II Oxidase{triangledown} ,{dagger}

M. Bekker,1* S. de Vries,2 A. Ter Beek,1 K. J. Hellingwerf,1 and M. J. Teixeira de Mattos1

Molecular Microbial Physiology Group, Swammerdam Institute for Life Sciences, BioCentrum, University of Amsterdam, Nieuwe Achtergracht 166, 1018 WV Amsterdam,1 Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC, Delft, The Netherlands2

Received 28 April 2009/ Accepted 14 June 2009

The respiratory chain of Escherichia coli is usually considered a device to conserve energy via the generation of a proton motive force, which subsequently may drive ATP synthesis by the ATP synthetase. It is known that in this system a fixed amount of ATP per oxygen molecule reduced (P/O ratio) is not synthesized due to alternative NADH dehydrogenases and terminal oxidases with different proton pumping stoichiometries. Here we show that P/O ratios can vary much more than previously thought. First, we show that in wild-type E. coli cytochrome bo, cytochrome bd-I, and cytochrome bd-II are the major terminal oxidases; deletion of all of the genes encoding these enzymes results in a fermentative phenotype in the presence of oxygen. Second, we provide evidence that the electron flux through cytochrome bd-II oxidase is significant but does not contribute to the generation of a proton motive force. The kinetics support the view that this system is as an energy-independent system gives the cell metabolic flexibility by uncoupling catabolism from ATP synthesis under non-steady-state conditions. The nonelectrogenic nature of cytochrome bd-II oxidase implies that the respiratory chain can function in a fully uncoupled mode such that ATP synthesis occurs solely by substrate level phosphorylation. As a consequence, the yield with a carbon and energy source can vary five- to sevenfold depending on the electron flux distribution in the respiratory chain. A full understanding and control of this distribution open new avenues for optimization of biotechnological processes.

* Corresponding author. Mailing address: Swammerdam Institute for Life Sciences, BioCentrum, University of Amsterdam, Nieuwe Achtergracht 166, 1018 WV Amsterdam, The Netherlands. Phone: 31-20-5257066. E-mail: m.bekker{at}uva.nl

{triangledown} Published ahead of print on 19 June 2009.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, September 2009, p. 5510-5517, Vol. 191, No. 17
0021-9193/09/$08.00+0     doi:10.1128/JB.00562-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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