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Applied and Environmental Microbiology, February 2008, p. 1136-1144, Vol. 74, No. 4
0099-2240/08/$08.00+0     doi:10.1128/AEM.01061-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Contribution of Citrate Metabolism to the Growth of Lactococcus lactis CRL264 at Low pH{triangledown}

Claudia Sánchez,1 Ana Rute Neves,1 João Cavalheiro,1 Margarida Moreira dos Santos,1 Nieves García-Quintáns,2 Paloma López,2 and Helena Santos1*

Instituto de Tecnologia Química e Biológica/Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Apt. 127, 2780-156 Oeiras, Portugal,1 Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, CL Ramiro de Maeztu 9, 28040 Madrid, Spain2

Received 11 May 2007/ Accepted 16 December 2007

Lactococcus lactis subsp. lactis biovar diacetylactis CRL264 is a natural strain isolated from cheese (F. Sesma, D. Gardiol, A. P. de Ruiz Holgado, and D. de Mendoza, Appl. Environ. Microbiol. 56:2099-2103, 1990). The effect of citrate on the growth parameters at a very acidic pH value was studied with this strain and with derivatives whose citrate uptake capacity was genetically manipulated. The culture pH was maintained at 4.5 to prevent alkalinization of the medium, a well-known effect of citrate metabolism. In the presence of citrate, the maximum specific growth rate and the specific glucose consumption rate were stimulated. Moreover, a more efficient energy metabolism was revealed by analysis of the biomass yields relative to glucose consumption or ATP production. Thus, it was shown that the beneficial effect of citrate on growth under acid stress conditions is not primarily due to the concomitant alkalinization of the medium but stems from less expenditure of ATP, derived from glucose catabolism, to achieve pH homeostasis. After citrate depletion, a deleterious effect on the final biomass was apparent due to organic acid accumulation, particularly acetic acid. On the other hand, citrate metabolism endowed cells with extra ability to counteract lactic and acetic acid toxicity. In vivo 13C nuclear magnetic resonance provided strong evidence for the operation of a citrate/lactate exchanger. Interestingly, the greater capacity for citrate transport correlated positively with the final biomass and growth rates of the citrate-utilizing strains. We propose that increasing the citrate transport capacity of CRL264 could be a useful strategy to improve further the ability of this strain to cope with strongly acidic conditions.

* Corresponding author. Mailing address: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande, 6, Apt. 127, 2780-156 Oeiras, Portugal. Phone: 351-214469828. Fax: 351-214428766. E-mail: santos{at}itqb.unl.pt

{triangledown} Published ahead of print on 21 December 2007.

Applied and Environmental Microbiology, February 2008, p. 1136-1144, Vol. 74, No. 4
0099-2240/08/$08.00+0     doi:10.1128/AEM.01061-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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