Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Jun;178(11):3127–3132. doi: 10.1128/jb.178.11.3127-3132.1996

The proton motive force generated in Leuconostoc oenos by L-malate fermentation.

M Salema 1, J S Lolkema 1, M V San Romão 1, M C Lourero Dias 1
PMCID: PMC178062  PMID: 8655490

Abstract

In cells of Leuconostoc oenos, the fermentation of L-malic acid generates both a transmembrane pH gradient, inside alkaline, and an electrical potential gradient, inside negative. In resting cells, the proton motive force ranged from -170 mV to -88 mV between pH 3.1 and 5.6 in the presence Of L-malate. Membrane potentials were calculated by using a model for probe binding that accounted for the different binding constants at the different pH values at the two faces of the membrane. The delta psi generated by the transport of monovalent malate, H-malate-, controlled the rate of fermentation. The fermentation rate significantly increased under conditions of decreased delta psi, i.e., upon addition of the ionophore valinomycin in the presence of KCl, whereas in a buffer depleted of potassium, the addition of valinomycin resulted in a hyperpolarization of the cell membrane and a reduction of the rate of fermentation. At the steady state, the chemical gradient for H-malate- was of the same magnitude as delta psi. Synthesis of ATP was observed in cells performing malolactic fermentation.

Full Text

The Full Text of this article is available as a PDF (323.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anantharam V., Allison M. J., Maloney P. C. Oxalate:formate exchange. The basis for energy coupling in Oxalobacter. J Biol Chem. 1989 May 5;264(13):7244–7250. [PubMed] [Google Scholar]
  2. Booth I. R. Regulation of cytoplasmic pH in bacteria. Microbiol Rev. 1985 Dec;49(4):359–378. doi: 10.1128/mr.49.4.359-378.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dicks L. M., Dellaglio F., Collins M. D. Proposal to reclassify Leuconostoc oenos as Oenococcus oeni [corrig.] gen. nov., comb. nov.. Int J Syst Bacteriol. 1995 Apr;45(2):395–397. doi: 10.1099/00207713-45-2-395. [DOI] [PubMed] [Google Scholar]
  4. Harold F. M., Van Brunt J. Circulation of H+ and K+ across the plasma membrane is not obligatory for bacterial growth. Science. 1977 Jul 22;197(4301):372–373. doi: 10.1126/science.69317. [DOI] [PubMed] [Google Scholar]
  5. Hugenholtz J., Perdon L., Abee T. Growth and Energy Generation by Lactococcus lactis subsp. lactis biovar diacetylactis during Citrate Metabolism. Appl Environ Microbiol. 1993 Dec;59(12):4216–4222. doi: 10.1128/aem.59.12.4216-4222.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kamo N., Muratsugu M., Hongoh R., Kobatake Y. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol. 1979 Aug;49(2):105–121. doi: 10.1007/BF01868720. [DOI] [PubMed] [Google Scholar]
  7. Kashket E. R. The proton motive force in bacteria: a critical assessment of methods. Annu Rev Microbiol. 1985;39:219–242. doi: 10.1146/annurev.mi.39.100185.001251. [DOI] [PubMed] [Google Scholar]
  8. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  9. Lolkema J. S., Abbing A., Hellingwerf K. J., Konings W. N. The transmembrane electrical potential in Rhodopseudomonas sphaeroides determined from the distribution of tetraphenylphosphonium after correction for its binding to cell components. Eur J Biochem. 1983 Feb 1;130(2):287–292. doi: 10.1111/j.1432-1033.1983.tb07149.x. [DOI] [PubMed] [Google Scholar]
  10. Loubiere P., Salou P., Leroy M. J., Lindley N. D., Pareilleux A. Electrogenic malate uptake and improved growth energetics of the malolactic bacterium Leuconostoc oenos grown on glucose-malate mixtures. J Bacteriol. 1992 Aug;174(16):5302–5308. doi: 10.1128/jb.174.16.5302-5308.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lundin A., Thore A. Comparison of methods for extraction of bacterial adenine nucleotides determined by firefly assay. Appl Microbiol. 1975 Nov;30(5):713–721. doi: 10.1128/am.30.5.713-721.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Molenaar D., Bosscher J. S., ten Brink B., Driessen A. J., Konings W. N. Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J Bacteriol. 1993 May;175(10):2864–2870. doi: 10.1128/jb.175.10.2864-2870.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Olsen E. B., Russell J. B., Henick-Kling T. Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation. J Bacteriol. 1991 Oct;173(19):6199–6206. doi: 10.1128/jb.173.19.6199-6206.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Otto R., Sonnenberg A. S., Veldkamp H., Konings W. N. Generation of an electrochemical proton gradient in Streptococcus cremoris by lactate efflux. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5502–5506. doi: 10.1073/pnas.77.9.5502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Poolman B., Molenaar D., Smid E. J., Ubbink T., Abee T., Renault P. P., Konings W. N. Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J Bacteriol. 1991 Oct;173(19):6030–6037. doi: 10.1128/jb.173.19.6030-6037.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Poolman B. Precursor/product antiport in bacteria. Mol Microbiol. 1990 Oct;4(10):1629–1636. doi: 10.1111/j.1365-2958.1990.tb00539.x. [DOI] [PubMed] [Google Scholar]
  17. Ritchey T. W., Seely H. W., Jr Distribution of cytochrome-like respiration in streptococci. J Gen Microbiol. 1976 Apr;93(2):195–203. doi: 10.1099/00221287-93-2-195. [DOI] [PubMed] [Google Scholar]
  18. Rottenberg H. The measurement of membrane potential and deltapH in cells, organelles, and vesicles. Methods Enzymol. 1979;55:547–569. doi: 10.1016/0076-6879(79)55066-6. [DOI] [PubMed] [Google Scholar]
  19. Salema M., Poolman B., Lolkema J. S., Dias M. C., Konings W. N. Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc oenos. Eur J Biochem. 1994 Oct 1;225(1):289–295. doi: 10.1111/j.1432-1033.1994.00289.x. [DOI] [PubMed] [Google Scholar]
  20. Simpson S. J., Bendall M. R., Egan A. F., Vink R., Rogers P. J. High-field phosphorus NMR studies of the stoichiometry of the lactate/proton carrier in Streptococcus faecalis. Eur J Biochem. 1983 Oct 17;136(1):63–69. doi: 10.1111/j.1432-1033.1983.tb07705.x. [DOI] [PubMed] [Google Scholar]
  21. Ten Brink B., Konings W. N. Generation of an electrochemical proton gradient by lactate efflux in membrane vesicles of Escherichia coli. Eur J Biochem. 1980 Oct;111(1):59–66. doi: 10.1111/j.1432-1033.1980.tb06074.x. [DOI] [PubMed] [Google Scholar]
  22. Zaritsky A., Kihara M., Macnab R. M. Measurement of membrane potential in Bacillus subtilis: a comparison of lipophilic cations, rubidium ion, and a cyanine dye as probes. J Membr Biol. 1981;63(3):215–231. doi: 10.1007/BF01870983. [DOI] [PubMed] [Google Scholar]
  23. ten Brink B., Konings W. N. Electrochemical proton gradient and lactate concentration gradient in Streptococcus cremoris cells grown in batch culture. J Bacteriol. 1982 Nov;152(2):682–686. doi: 10.1128/jb.152.2.682-686.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. ten Brink B., Otto R., Hansen U. P., Konings W. N. Energy recycling by lactate efflux in growing and nongrowing cells of Streptococcus cremoris. J Bacteriol. 1985 Apr;162(1):383–390. doi: 10.1128/jb.162.1.383-390.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES