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. 1991 Apr;57(4):941–944. doi: 10.1128/aem.57.4.941-944.1991

Lactose Uptake Driven by Galactose Efflux in Streptococcus thermophilus: Evidence for a Galactose-Lactose Antiporter †

Robert W Hutkins 1,*, Carina Ponne 1
PMCID: PMC182826  PMID: 16348472

Abstract

Galactose-nonfermenting (Gal-) Streptococcus thermophilus TS2 releases galactose into the extracellular medium when grown in medium containing excess lactose. Starved and de-energized Gal- cells, however, could be loaded with galactose to levels approximately equal to the extracellular concentration (0 to 50 mM). When loaded cells were separated from the medium and resuspended in fresh broth containing 5 mM lactose, galactose efflux occurred. De-energized, galactose-loaded cells, resuspended in buffer or medium, accumulated [14C]lactose at a greater rate and to significantly higher intracellular concentrations than unloaded cells. Uptake of lactose by loaded cells was inhibited more than that by unloaded cells in the presence of extracellular galactose, indicating that a galactose gradient was involved in the exchange system. When de-energized, galactose-loaded cells were resuspended in carbohydrate-free medium at pH 6.7, a proton motive force (Δp) of 86 to 90 mV was formed, whereas de-energized, nonloaded cells maintained a Δp of about 56 mV. However, uptake of lactose by loaded cells occurred when the proton motive force was abolished by the addition of an uncoupler or in the presence of a proton-translocating ATPase inhibitor. These results support the hypothesis that galactose efflux in Gal-S. thermophilus is electrogenic and that the exchange reaction (lactose uptake and galactose efflux) probably occurs via an antiporter system.

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Selected References

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  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. Bentaboulet M., Robin A., Kepes A. Artificially induced active transport of amino acid driven by the efflux of a sugar via a heterologous transport system in de-energized Escherichia coli. Biochem J. 1979 Jan 15;178(1):103–107. doi: 10.1042/bj1780103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cox D. J., Henick-Kling T. Chemiosmotic energy from malolactic fermentation. J Bacteriol. 1989 Oct;171(10):5750–5752. doi: 10.1128/jb.171.10.5750-5752.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Driessen A. J., Poolman B., Kiewiet R., Konings W. Arginine transport in Streptococcus lactis is catalyzed by a cationic exchanger. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6093–6097. doi: 10.1073/pnas.84.17.6093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Driessen A. J., Smid E. J., Konings W. N. Transport of diamines by Enterococcus faecalis is mediated by an agmatine-putrescine antiporter. J Bacteriol. 1988 Oct;170(10):4522–4527. doi: 10.1128/jb.170.10.4522-4527.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Flagg J. L., Wilson T. H. A novel type of coupling between proline and galactoside transport in Escherichia coli. Membr Biochem. 1978;1(1-2):61–72. doi: 10.3109/09687687809064159. [DOI] [PubMed] [Google Scholar]
  7. Hutkins R. W., Kashket E. R. Phosphotransferase Activity in Clostridium acetobutylicum from Acidogenic and Solventogenic Phases of Growth. Appl Environ Microbiol. 1986 May;51(5):1121–1123. doi: 10.1128/aem.51.5.1121-1123.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hutkins R., Morris H. A., McKay L. L. Galactokinase activity in Streptococcus thermophilus. Appl Environ Microbiol. 1985 Oct;50(4):777–780. doi: 10.1128/aem.50.4.777-780.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hutkins R., Morris H. A., McKay L. L. Galactose transport in Streptococcus thermophilus. Appl Environ Microbiol. 1985 Oct;50(4):772–776. doi: 10.1128/aem.50.4.772-776.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kashket E. R., Blanchard A. G., Metzger W. C. Proton motive force during growth of Streptococcus lactis cells. J Bacteriol. 1980 Jul;143(1):128–134. doi: 10.1128/jb.143.1.128-134.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Maloney P. C., Ambudkar S. V., Thomas J., Schiller L. Phosphate/hexose 6-phosphate antiport in Streptococcus lactis. J Bacteriol. 1984 Apr;158(1):238–245. doi: 10.1128/jb.158.1.238-245.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maloney P. C. Microbes and membrane biology. FEMS Microbiol Rev. 1990 Sep;7(1-2):91–102. doi: 10.1111/j.1574-6968.1990.tb04881.x. [DOI] [PubMed] [Google Scholar]
  13. O'leary V. S., Woychik J. H. Utilization of Lactose, Glucose, and Galactose by a Mixed Culture of Streptococcus thermophilus and Lactobacillus bulgaricus in Milk Treated with Lactase Enzyme. Appl Environ Microbiol. 1976 Jul;32(1):89–94. doi: 10.1128/aem.32.1.89-94.1976. [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., Royer T. J., Mainzer S. E., Schmidt B. F. Carbohydrate utilization in Streptococcus thermophilus: characterization of the genes for aldose 1-epimerase (mutarotase) and UDPglucose 4-epimerase. J Bacteriol. 1990 Jul;172(7):4037–4047. doi: 10.1128/jb.172.7.4037-4047.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Poolman B., Royer T. J., Mainzer S. E., Schmidt B. F. Lactose transport system of Streptococcus thermophilus: a hybrid protein with homology to the melibiose carrier and enzyme III of phosphoenolpyruvate-dependent phosphotransferase systems. J Bacteriol. 1989 Jan;171(1):244–253. doi: 10.1128/jb.171.1.244-253.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Thomas T. D., Crow V. L. Selection of Galactose-Fermenting Streptococcus thermophilus in Lactose-Limited Chemostat Cultures. Appl Environ Microbiol. 1984 Jul;48(1):186–191. doi: 10.1128/aem.48.1.186-191.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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