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. 1969 Apr;98(1):198–204. doi: 10.1128/jb.98.1.198-204.1969

Energy Coupling in the Transport of β-Galactosides by Escherichia Coli: Effect of Proton Conductors

Emilie Pavlasova a,1, F M Harold a
PMCID: PMC249923  PMID: 4889268

Abstract

Escherichia coli accumulates thiomethyl-β-d-galactoside against a concentration gradient under anaerobic conditions. The accumulation was abolished by carbonylcyanide m-chlorophenylhydrazone, tetrachlorosalicylanilide, 2,4 dinitrophenol, and other uncouplers of oxidative phosphorylation even though oxidative phosphorylation would not be expected to occur anaerobically. In the presence of the uncouplers, the β-galactoside carrier remained functional and catalyzed equilibration of thiomethylgalactoside across the membrane. The uncouplers did not inhibit the generation of adenosine triphosphate or protein turnover, or the accumulation of α-methylglucoside and glycerol by phosphorylation. We conclude that, at least anaerobically, uncouplers of oxidative phosphorylation do not interfere with energy metabolism in general, but prevent the utilization of metabolic energy for the active transport of galactosides. The uncouplers also facilitate passage of protons across the membrane. Various hypotheses are considered to explain why a proton-impermeable membrane may be required for active transport of galactosides and other substrates.

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Selected References

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

  1. BUTTIN G., COHEN G. N., MONOD J., RICKENBERG H. V. La galactoside-perméase d'Escherichia coli. Ann Inst Pasteur (Paris) 1956 Dec;91(6):829–857. [PubMed] [Google Scholar]
  2. Carafoli E., Rossi C. S. The effect of dinitrophenol on the permeability of the mitochondrial membrane. Biochem Biophys Res Commun. 1967 Oct 26;29(2):153–157. doi: 10.1016/0006-291x(67)90579-7. [DOI] [PubMed] [Google Scholar]
  3. DAWES E. A., RIBBONS D. W. SOME ASPECTS OF THE ENDOGENOUS METABOLISM OF BACTERIA. Bacteriol Rev. 1964 Jun;28:126–149. doi: 10.1128/br.28.2.126-149.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. FORREST W. W., WALKER D. J. SYNTHESIS OF RESERVE MATERIALS FOR ENDOGENOUS METABOLISM IN STREPTOCOCCUS FAECALIS. J Bacteriol. 1965 Jun;89:1448–1452. doi: 10.1128/jb.89.6.1448-1452.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fox C. F., Carter J. R., Kennedy E. P. GENETIC CONTROL OF THE MEMBRANE PROTEIN COMPONENT OF THE LACTOSE TRANSPORT SYSTEM OF Escherichia coli. Proc Natl Acad Sci U S A. 1967 Mar;57(3):698–705. doi: 10.1073/pnas.57.3.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fox C. F., Kennedy E. P. Specific labeling and partial purification of the M protein, a component of the beta-galactoside transport system of Escherichia coli. Proc Natl Acad Sci U S A. 1965 Sep;54(3):891–899. doi: 10.1073/pnas.54.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. HAYASHI S., LIN E. C. CAPTURE OF GLYCEROL BY CELLS OF ESCHERICHIA COLI. Biochim Biophys Acta. 1965 Mar 29;94:479–487. doi: 10.1016/0926-6585(65)90056-7. [DOI] [PubMed] [Google Scholar]
  8. HOFFEE P., ENGLESBERG E., LAMY F. THE GLUCOSE PERMEASE SYSTEM IN BACTERIA. Biochim Biophys Acta. 1964 Mar 30;79:337–350. [PubMed] [Google Scholar]
  9. Hamilton W. A. The mechanism of the bacteriostatic action of tetrachlorosalicylanilide: a Membrane-active antibacterial compound. J Gen Microbiol. 1968 Mar;50(3):441–458. doi: 10.1099/00221287-50-3-441. [DOI] [PubMed] [Google Scholar]
  10. Harold F. M., Baarda J. R. Gramicidin, valinomycin, and cation permeability of Streptococcus faecalis. J Bacteriol. 1967 Jul;94(1):53–60. doi: 10.1128/jb.94.1.53-60.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harold F. M., Baarda J. R. Inhibition of membrane transport in Streptococcus faecalis by uncouplers of oxidative phosphorylation and its relationship to proton conduction. J Bacteriol. 1968 Dec;96(6):2025–2034. doi: 10.1128/jb.96.6.2025-2034.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harris E. J., Höfer M. P., Pressman B. C. Stimulation of mitochondrial respiration and phosphorylation by transport-inducing antibiotics. Biochemistry. 1967 May;6(5):1348–1360. doi: 10.1021/bi00857a018. [DOI] [PubMed] [Google Scholar]
  13. Harris R. A., Penniston J. T., Asai J., Green D. E. The conformational basis of energy conservation in membrane systems. II. Correlation between conformational change and functional states. Proc Natl Acad Sci U S A. 1968 Mar;59(3):830–837. doi: 10.1073/pnas.59.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hopfer U., Lehninger A. L., Thompson T. E. Protonic conductance across phospholipid bilayer membranes induced by uncoupling agents for oxidative phosphorylation. Proc Natl Acad Sci U S A. 1968 Feb;59(2):484–490. doi: 10.1073/pnas.59.2.484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. KOCH A. L. THE ROLE OF PERMEASE IN TRANSPORT. Biochim Biophys Acta. 1964 Jan 27;79:177–200. doi: 10.1016/0926-6577(64)90050-6. [DOI] [PubMed] [Google Scholar]
  16. Kaback H. R. The role of the phosphoenolpyruvate-phosphotransferase system in the transport of sugars by isolated membrane preparations of Escherichia coli. J Biol Chem. 1968 Jul 10;243(13):3711–3724. [PubMed] [Google Scholar]
  17. Lehninger A. L., Carafoli E., Rossi C. S. Energy-linked ion movements in mitochondrial systems. Adv Enzymol Relat Areas Mol Biol. 1967;29:259–320. doi: 10.1002/9780470122747.ch6. [DOI] [PubMed] [Google Scholar]
  18. Leive L. Studies on the permeability change produced in coliform bacteria by ethylenediaminetetraacetate. J Biol Chem. 1968 May 10;243(9):2373–2380. [PubMed] [Google Scholar]
  19. MONOD J., COHEN-BAZIRE G., COHN M. Sur la biosynthèse de la beta-galactosidase (lactase) chez Escherichia coli; la spécificité de l'induction. Biochim Biophys Acta. 1951 Nov;7(4):585–599. doi: 10.1016/0006-3002(51)90072-8. [DOI] [PubMed] [Google Scholar]
  20. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc. 1966 Aug;41(3):445–502. doi: 10.1111/j.1469-185x.1966.tb01501.x. [DOI] [PubMed] [Google Scholar]
  21. Mitchell P., Moyle J. Acid-base titration across the membrane system of rat-liver mitochondria. Catalysis by uncouplers. Biochem J. 1967 Aug;104(2):588–600. doi: 10.1042/bj1040588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mitchell P. Proton-translocation phosphorylation in mitochondria, chloroplasts and bacteria: natural fuel cells and solar cells. Fed Proc. 1967 Sep;26(5):1370–1379. [PubMed] [Google Scholar]
  23. Neu H. C., Heppel L. A. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J Biol Chem. 1965 Sep;240(9):3685–3692. [PubMed] [Google Scholar]
  24. Scarborough G. A., Rumley M. K., Kennedy E. P. The function of adenosine 5'-triphosphate in the lactose transport system of Escherichia coli. Proc Natl Acad Sci U S A. 1968 Jul;60(3):951–958. doi: 10.1073/pnas.60.3.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Simoni R. D., Levinthal M., Kundig F. D., Kundig W., Anderson B., Hartman P. E., Roseman S. Genetic evidence for the role of a bacterial phosphotransferase system in sugar transport. Proc Natl Acad Sci U S A. 1967 Nov;58(5):1963–1970. doi: 10.1073/pnas.58.5.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tanaka S., Fraenkel D. G., Lin E. C. The enzymatic lesion of strain MM-6, a pleiotropic carbohydrate-negative mutant of Escherichia coli. Biochem Biophys Res Commun. 1967 Apr 7;27(1):63–67. doi: 10.1016/s0006-291x(67)80040-8. [DOI] [PubMed] [Google Scholar]
  27. WILBRANDT W., ROSENBERG T. The concept of carrier transport and its corollaries in pharmacology. Pharmacol Rev. 1961 Jun;13:109–183. [PubMed] [Google Scholar]
  28. Weinbach E. C., Garbus J. Structural changes in mitochondria induced by uncoupling reagents. The response to proteolytic enzymes. Biochem J. 1968 Feb;106(3):711–717. doi: 10.1042/bj1060711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Winkler H. H., Wilson T. H. The role of energy coupling in the transport of beta-galactosides by Escherichia coli. J Biol Chem. 1966 May 25;241(10):2200–2211. [PubMed] [Google Scholar]
  30. Woodroffe R. C., Wilkinson B. E. The antibacterial action of tetrachlorsalicylanilide. J Gen Microbiol. 1966 Sep;44(3):343–352. doi: 10.1099/00221287-44-3-343. [DOI] [PubMed] [Google Scholar]

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