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. 1974 Oct;71(10):3896–3900. doi: 10.1073/pnas.71.10.3896

A Protonmotive Force Drives ATP Synthesis in Bacteria

Peter C Maloney 1, E R Kashket 1, T Hastings Wilson 1
PMCID: PMC434292  PMID: 4279406

Abstract

When cells of Streptococcus lactis or Escherichia coli were suspended in a potassium-free medium, a membrane potential (negative inside) could be artificially generated by the addition of the potassium ionophore, valinomycin. In response to this inward directed protonmotive force, ATP synthesis catalyzed by the membrane-bound ATPase (EC 3.6.1.3) was observed. The formation of ATP was not found in S. lactis that had been treated with the ATPase inhibitor, N,N′-dicyclohexylcarbodiimide, nor was it observed in a mutant of E. coli lacking the ATPase. Inhibition of ATP synthesis in S. lactis was also observed when the membrane potential was reduced by the presence of external potassium, or when cells were first incubated with the proton conductor, carbonylcyanidefluoromethoxyphenylhydrazone. These results are in agreement with predictions made by the chemiosmotic hypothesis of Mitchell.

Keywords: chemiosmotic hypothesis, membrane-bound ATPase, membrane potential, valinomycin, ATPase-negative mutants

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Selected References

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

  1. Asghar S. S., Levin E., Harold F. M. Accumulation of neutral amino acids by Streptococcus faecalis. Energy coupling by a proton-motive force. J Biol Chem. 1973 Aug 10;248(15):5225–5233. [PubMed] [Google Scholar]
  2. Berger E. A. Different mechanisms of energy coupling for the active transport of proline and glutamine in Escherichia coli. Proc Natl Acad Sci U S A. 1973 May;70(5):1514–1518. doi: 10.1073/pnas.70.5.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Butlin J. D., Cox G. B., Gibson F. Oxidative phosphorylation in Escherichia coli K12. Mutations affecting magnesium ion- or calcium ion-stimulated adenosine triphosphatase. Biochem J. 1971 Aug;124(1):75–81. doi: 10.1042/bj1240075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cockrell R. S., Harris E. J., Pressman B. C. Synthesis of ATP driven by a potassium gradient in mitochondria. Nature. 1967 Sep 30;215(5109):1487–1488. doi: 10.1038/2151487a0. [DOI] [PubMed] [Google Scholar]
  5. Cole H. A., Wimpenny J. W., Hughes D. E. The ATP pool in Escherichia coli. I. Measurement of the pool using modified luciferase assay. Biochim Biophys Acta. 1967;143(3):445–453. doi: 10.1016/0005-2728(67)90050-3. [DOI] [PubMed] [Google Scholar]
  6. Cox G. B., Newton N. A., Butlin J. D., Gibson F. The energy-linked transhydrogenase reaction in respiratory mutants of Escherichia coli K12. Biochem J. 1971 Nov;125(2):489–493. doi: 10.1042/bj1250489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Evans D. J. Membrane Mg-(Ca)-Activated Adenosine Triphosphatase of Escherichia coli: Characterization in the Membrane-Bound and Solubilized States. J Bacteriol. 1970 Dec;104(3):1203–1212. doi: 10.1128/jb.104.3.1203-1212.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garrahan P. J., Glynn I. M. Driving the sodium pump backwards to form adenosine triphosphate. Nature. 1966 Sep 24;211(5056):1414–1415. doi: 10.1038/2111414a0. [DOI] [PubMed] [Google Scholar]
  9. Glynn I. M. Involvement of a membrane potential in the synthesis of ATP by mitochondria. Nature. 1967 Dec 30;216(5122):1318–1319. doi: 10.1038/2161318a0. [DOI] [PubMed] [Google Scholar]
  10. Harold F. M., Baarda J. R., Baron C., Abrams A. Inhibition of membrane-bound adenosine triphosphatase and of cation transport in Streptococcus faecalis by N,N'-dicyclohexylcarbodiimide. J Biol Chem. 1969 May 10;244(9):2261–2268. [PubMed] [Google Scholar]
  11. Harold F. M. Conservation and transformation of energy by bacterial membranes. Bacteriol Rev. 1972 Jun;36(2):172–230. doi: 10.1128/br.36.2.172-230.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harold F. M., Papineau D. Cation transport and electrogenesis by Streptococcus faecalis. I. The membrane potential. J Membr Biol. 1972;8(1):27–44. doi: 10.1007/BF01868093. [DOI] [PubMed] [Google Scholar]
  13. Harold F. M., Papineau D. Cation transport and electrogenesis by Streptococcus faecalis. II. Proton and sodium extrusion. J Membr Biol. 1972;8(1):45–62. doi: 10.1007/BF01868094. [DOI] [PubMed] [Google Scholar]
  14. Harold F. M., Pavlasová E., Baarda J. R. A transmembrane pH gradient in Streptococcus faecalis: origin, and dissipation by proton conductors and N,N'-dicyclohexylcarbodimide. Biochim Biophys Acta. 1970;196(2):235–244. doi: 10.1016/0005-2736(70)90011-8. [DOI] [PubMed] [Google Scholar]
  15. Jagendorf A. T., Uribe E. ATP formation caused by acid-base transition of spinach chloroplasts. Proc Natl Acad Sci U S A. 1966 Jan;55(1):170–177. doi: 10.1073/pnas.55.1.170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kanner B. I., Gutnick D. L. Energy linked nicotinamide adenine dinucleotide transhydrogenase in a mutant of Escherichia coli K12 lacking membrane Mg(2+)&z.sbnd;Ca(2+)-activated adenosine triphosphatase. FEBS Lett. 1972 May 1;22(2):197–199. doi: 10.1016/0014-5793(72)80043-7. [DOI] [PubMed] [Google Scholar]
  17. Kanner B. I., Gutnick D. L. Use of neomycin in the isolation of mutants blocked in energy conservation in Escherichia coli. J Bacteriol. 1972 Jul;111(1):287–289. doi: 10.1128/jb.111.1.287-289.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kashket E. R., Wilson T. H. Galactoside accumulation associated with ion movements in Streptococcus lactis. Biochem Biophys Res Commun. 1972 Nov 1;49(3):615–620. doi: 10.1016/0006-291x(72)90455-x. [DOI] [PubMed] [Google Scholar]
  19. Kashket E. R., Wilson T. H. Proton-coupled accumulation of galactoside in Streptococcus lactis 7962. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2866–2869. doi: 10.1073/pnas.70.10.2866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kashket E. R., Wilson T. H. Role of metabolic energy in the transport of -galactosides by Streptococcus lactis. J Bacteriol. 1972 Feb;109(2):784–789. doi: 10.1128/jb.109.2.784-789.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Klein W. L., Boyer P. D. Energization of active transport by Escherichia coli. J Biol Chem. 1972 Nov 25;247(22):7257–7265. [PubMed] [Google Scholar]
  22. Koch A. L. Energy expenditure is obligatory for the downhill transport of galactosides. J Mol Biol. 1971 Aug 14;59(3):447–459. doi: 10.1016/0022-2836(71)90309-3. [DOI] [PubMed] [Google Scholar]
  23. MITCHELL P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 1961 Jul 8;191:144–148. doi: 10.1038/191144a0. [DOI] [PubMed] [Google Scholar]
  24. Makinose M., Hasselbach W. ATP synthesis by the reverse of the sarcoplasmic calcium pump. FEBS Lett. 1971 Jan 30;12(5):271–272. doi: 10.1016/0014-5793(71)80196-5. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Racker E., Stoeckenius W. Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J Biol Chem. 1974 Jan 25;249(2):662–663. [PubMed] [Google Scholar]
  27. Reid R. A., Moyle J., Mitchell P. Synthesis of adenosine triphosphate by a protonmotive force in rat liver mitochondria. Nature. 1966 Oct 15;212(5059):257–258. doi: 10.1038/212257a0. [DOI] [PubMed] [Google Scholar]
  28. Rossi E., Azzone G. F. The mechanism of ion translocation in mitochondria. 3. Coupling of K+ efflux with ATP synthesis. Eur J Biochem. 1970 Feb;12(2):319–327. doi: 10.1111/j.1432-1033.1970.tb00853.x. [DOI] [PubMed] [Google Scholar]
  29. Schairer H. U., Haddock B. A. -Galactoside accumulation in a Mg 2+ -,Ca 2+ -activated ATPase deficient mutant of E.coli. Biochem Biophys Res Commun. 1972 Aug 7;48(3):544–551. doi: 10.1016/0006-291x(72)90382-8. [DOI] [PubMed] [Google Scholar]
  30. Scholes P., Mitchell P. Acid-base titration across the plasma membrane of Micrococcus denitrificans: factors affecting the effective proton conductance and the respiratory rate. J Bioenerg. 1970 Jun;1(1):61–72. doi: 10.1007/BF01516089. [DOI] [PubMed] [Google Scholar]
  31. Schuldiner S., Rottenberg H., Avron M. Membrane potential as a driving force for ATP synthesis in chloroplasts. FEBS Lett. 1972 Dec 1;28(2):173–176. doi: 10.1016/0014-5793(72)80704-x. [DOI] [PubMed] [Google Scholar]
  32. Simoni R. D., Shallenberger M. K. Coupling of energy to active transport of amino acids in Escherichia coli. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2663–2667. doi: 10.1073/pnas.69.9.2663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. West I. C., Mitchell P. The proton-translocating ATPase of Escherichia coli. FEBS Lett. 1974 Mar 15;40(1):1–4. doi: 10.1016/0014-5793(74)80880-x. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Yamamoto T. H., Mével-Ninio M., Valentine R. C. Essential role of membrane ATPase or coupling factor for anaerobic growth and anaerobic active transport in Escherichia coli. Biochim Biophys Acta. 1973 Sep 26;314(3):267–275. doi: 10.1016/0005-2728(73)90111-4. [DOI] [PubMed] [Google Scholar]

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