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Appl Environ Microbiol, May 1998, p. 1594-1600, Vol. 64, No. 5
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Mechanism of the Citrate Transporters in Carbohydrate and Citrate Cometabolism in Lactococcus and Leuconostoc Species

M. Bandell,1 M. E. Lhotte,2 C. Marty-Teysset,1,2 A. Veyrat,1 H. Prévost,2 V. Dartois,2 C. Diviès,2 W. N. Konings,1 and J. S. Lolkema1,*

Department of Microbiology, Groningen Biotechnology and Biomolecular Sciences Institute, University of Groningen, 9751NN Haren, The Netherlands,1 and Departement de Microbiologie-Biotechnologie, ENS-BANA, Université de Bourgogne, 21000 Dijon, France2

Received 11 November 1997/Accepted 9 February 1998

Citrate metabolism in the lactic acid bacterium Leuconostoc mesenteroides generates an electrochemical proton gradient across the membrane by a secondary mechanism (C. Marty-Teysset, C. Posthuma, J. S. Lolkema, P. Schmitt, C. Divies, and W. N. Konings, J. Bacteriol. 178:2178-2185, 1996). Reports on the energetics of citrate metabolism in the related organism Lactococcus lactis are contradictory, and this study was performed to clarify this issue. Cloning of the membrane potential-generating citrate transporter (CitP) of Leuconostoc mesenteroides revealed an amino acid sequence that is almost identical to the known sequence of the CitP of Lactococcus lactis. The cloned gene was expressed in a Lactococcus lactis Cit- strain, and the gene product was functionally characterized in membrane vesicles. Uptake of citrate was counteracted by the membrane potential, and the transporter efficiently catalyzed heterologous citrate-lactate exchange. These properties are essential for generation of a membrane potential under physiological conditions and show that the Leuconostoc CitP retains its properties when it is embedded in the cytoplasmic membrane of Lactococcus lactis. Furthermore, using the same criteria and experimental approach, we demonstrated that the endogenous CitP of Lactococcus lactis has the same properties, showing that the few differences in the amino acid sequences of the CitPs of members of the two genera do not result in different catalytic mechanisms. The results strongly suggest that the energetics of citrate degradation in Lactococcus lactis and Leuconostoc mesenteroides are the same; i.e., citrate metabolism in Lactococcus lactis is a proton motive force-generating process.

* Corresponding author. Mailing address: Department of Microbiology, Biological Centre, Kerklaan 30, 9751NN Haren, The Netherlands. Phone: 31-50-3632155. Fax: 31-50-3632154. E-mail: j.s.lolkema{at}biol.rug.nl.

Appl Environ Microbiol, May 1998, p. 1594-1600, Vol. 64, No. 5
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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