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The Journal of Membrane Biology

, Volume 60, Issue 2, pp 95–104 | Cite as

Bacteriorhodopsin in liposomes: Quantitative evaluation of ΔpH changes induced by variations of light intensity and conductivity parameters

  • Jos C. Arents
  • Klaas J. Hellingwerf
  • Karel van Dam
  • Hans V. Westerhoff
Articles

Summary

A description of ion movement and energy transduction in terms of a kinetic variant of nonequilibrium thermodynamics was subjected to experimental tests in bacteriorhodopsin liposomes. The effects of variation of light intensity, proton permeability, proton-potassium ion exchange activity, and potassium ion permeability on the steadystate pH gradient were in quantitative agreement with the predictions of the theoretical description. It is suggested that the theoretical description will be useful in other, more complex systems to gain detailed information about their energy transduction and ion permeation properties.

Keywords

Light Intensity Human Physiology Exchange Activity Experimental Test Quantitative Evaluation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

S13

5-chloro-3-tert-butyl-2′-chloro-4′-nitrosalicylanilide 1799; (hexofluoro-acetonyl) acetone

Symbols Meaning Manipulated by

Aν

effective energy input of the photon constant

ΔpH

pH gradient (out-in) several methods

Le

nonproton electric permeation coefficient valinomycin

LHl

electric proton leakage coefficient protonophore

Ln

electroneutral proton permeation coefficient nigericin

Lν

activity of bacteriorhodopsin light intensity

n

number of protons pumped per photocycle constant

α

inward pumping fraction preparation method

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References

  1. Anraku, Y. 1979. A mechanism of uncoupler-mediated proton translocation in liposomal membrane.In: Structure and Function of Biomembranes. K. Yagi, editor. p. 193. Japan Scientific Societies Press, TokyoGoogle Scholar
  2. Azzone, G.F., Pozzan, T., Massari, S., Bragadin, M. 1978. Proton electrochemical gradient and rate of controlled respiration in mitochondria.Biochim. Biophys. Acta 501:296PubMedGoogle Scholar
  3. Colowick, S.P., Womack, F.C. 1969. Binding of diffusible molecules by macromolecules: Rapid measurement by rate of dialysis.J. Biol. Chem. 244:774PubMedGoogle Scholar
  4. Erecinska, M., Wilson, D.F. 1979. Cellular energy metabolism. Or a valuable predictive model?Trends Biochem. Sci. 4:N65Google Scholar
  5. Heinz, E. 1978. Mechanics and Energetics of Biological Transport. Springer, BerlinGoogle Scholar
  6. Hellingwerf, K.J. 1979. Structural and functional studies on lipid vesicles containing bacteriorhodopsin. Ph. D. Thesis, Veenstra-Visser, Groningen, The NetherlandsGoogle Scholar
  7. Hellingwerf, K.J., Arents, J.C., Scholte, B.J., Westerhoff, H.V. 1979. Bacteriorhodopsin in liposomes. II. Experimental evidence in support of a theoretical model.Biochim. Biophys. Acta 547:561PubMedGoogle Scholar
  8. Hellingwerf, K.J., Scholte, B.J., Van Dam, K. 1978a. Bacteriorhodopsin vesicles. An outline of the requirements for light-dependent H+ pumping.Biochim. Biophys. Acta 513:66PubMedGoogle Scholar
  9. Hellingwerf, K.J., Tegelaers, F.P.W., Westerhoff, H.V., Arents, J.C., Van Dam, K. 1978b. Structural and functional description of membrane vesicles containing the light-driven proton pump from the plasma membrane of the halophilic bacteriumHalobacterium halobium: bacteriorhodopsin.In: Energetics and Structure of Halophilic Microorganisms. S.R. Caplan and M. Ginzburg, editors. p. 283. Elsevier, AmsterdamGoogle Scholar
  10. Hill, T.L., 1979. Steady-state coupling of four membrane systems in mitochondrial oxidative phosphorylation.Proc. Natl. Acad. Sci. USA 76:2236PubMedGoogle Scholar
  11. Honig, B., Ebrey, T., Callender, R.H., Dinur, U., Ottolenghi, M. 1979. Photoisomerization, energy storage, and charge separation: A model for light energy transduction in visual pigments and bacteriorhodopsin.Proc. Natl. Acad. Sci. USA 76:2503PubMedGoogle Scholar
  12. Kagawa, Y., Racker, E. 1971. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XXV. Reconstitution of vesicles catalyzing32Pi-adenosine triphosphate exchange.J. Biol. Chem. 24:5477Google Scholar
  13. Katchalsky, A., Curran, P.F. 1967. Non-equilibrium thermodynamics in biophysics. Harvard University Press, Cambridge, Mass.Google Scholar
  14. Kell, D.B., Morris, J.G. 1980. Formulation and some biological uses of a buffer mixture whose buffering capacity is relatively independent of pH in the range pH 4–9.J. Biochem. Biophys. Meth. 3:143PubMedGoogle Scholar
  15. Keszthelyi, L., Ormos, P. 1980. Electric signals associated with the photocycle of bacteriorhodopsin.FEBS Lett. 109:189Google Scholar
  16. Mitchell, P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism.Nature 191:144PubMedGoogle Scholar
  17. Mitchell, P., Moyle, J. 1967. Acid-base titrations across the membrane system of rat-liver mitochondria. Catalysis by uncouplers.Biochem. J. 104:588PubMedGoogle Scholar
  18. Nicholls, D.G. 1974. The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined from ion distribution.Eur. J. Biochem. 50:305PubMedGoogle Scholar
  19. O'Brien, T.A., Nieva-Gomez, D., Gennis, R.B. 1978. Complex formation between the uncoupler carbonyl cyanidep-trifluoromethoxyphenylhydrazone (FCCP) and valinomycin in the presence of potassium.J. Biol. Chem. 253:1749PubMedGoogle Scholar
  20. Onsager, L. 1931. Reciprocal relations in irreversible processes. I.Phys. Rev. 37:405Google Scholar
  21. Ort, D.R., Parson, W.W. 1979. The quantum yield of flash-induced proton release by bacteriorhodopsin containing membrane fragments.Biophys. J. 25:34Google Scholar
  22. Ovchinnikov, Yu.A., Ivanov, V.T., Shkrob, A.M. 1974. Membrane Active Complexones. Elsevier, AmsterdamGoogle Scholar
  23. Padan, E., Rottenberg, H. 1973. Respiratory control and the proton electrochemical gradient in mitochondria.Eur. J. Biochem. 40:431PubMedGoogle Scholar
  24. Penefski, H.S. 1977. Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase.J. Biol. Chem. 522:2891Google Scholar
  25. Rott, R., Avi-Dor, Y. 1977. Effect of ionophoric compounds on aqueous suspensions of purple membranes.FEBS Lett. 81:267PubMedGoogle Scholar
  26. Rottenberg, H. 1973. The thermodynamic description of, enzymecatalyzed reactions. The linear relation between the reaction rate and the affinity.Biophys. J. 13:502Google Scholar
  27. Rottenberg, H. 1979. Non-equilibrium thermodynamics of energy conversion in bioenergetics.Biochim. Biophys. Acta 549:225PubMedGoogle Scholar
  28. Singh, K., Caplan, S.R. 1980. The purple membrane and solar energy conversion.Trends Biochem. Sci. 5:62Google Scholar
  29. Slater, E.C. 1977. Mechanism of oxidative phosphorylation.Annu. Rev. Biochem. 46:1015PubMedGoogle Scholar
  30. Sorgato, M.C., Ferguson, S.J. 1979. Variable proton conductance of submitochondrial particles.Biochemistry 18:5737PubMedGoogle Scholar
  31. Stoeckenius, W., Lozier, R.H., Bogomolni, R.A. 1979. Bacteriorhodopsin and the purple membrane of halobacteria.Biochim. Biophys. Acta 505:215PubMedGoogle Scholar
  32. Van Dam, K., Casey, R.A., Van der Meer, R., Groen, A.K., Westerhoff, H.V. 1978. The energy balance of oxidative phosphorylation.In: Frontiers of Biological Energetics. P.E. Dutton L.S. Leigh and A. Scarpa, editors Vol. 1, p. 430. Academic Press, New YorkGoogle Scholar
  33. Van Dam, K., Westerhoff, H.V. 1977. A description of oxidative phosphorylation in terms of irreversible thermodynamics.In: Structure and Function of Energy-Transducing Membranes. K. van Dam and B.F. van Gelder, editors. p. 157. Elsevier, AmsterdamGoogle Scholar
  34. Van Dam, K., Westerhoff, H.V., Krab, K., Van der Meer, R., Arents, J.C. 1980. Relationship between chemiosmotic flows and thermodynamic forces in oxidative phosphorylation.Biochim. Biophys. Acta 591:240PubMedGoogle Scholar
  35. Van der Meer, R., Westerhoff, H.V., Van Dam, K. 1980. Linear relations between rate and thermodynamic forces in enzymecatalyzed reactions.Biochim. Biophys. Acta 591:488PubMedGoogle Scholar
  36. Westerhoff, H.V., Hellingwerf, K.J., Arents, J.C., Scholte, B.J., Van Dam, K. 1981. Mosaic non-equilibrium thermodynamics describes biological energy transduction.Proc. Natl. Acad. Sci. USA (in press) Google Scholar
  37. Westerhoff, H.V., Scholte, B.J., Hellingwerf, K.J. 1979. Bacteriorhodopsin in liposomes. I. A description using irreversible thermodynamics.Biochim. Biophys. Acta 547:544PubMedGoogle Scholar
  38. Westerhoff, H.V., Van Dam, K. 1979. Irreversible thermodynamic description of energy transduction in biomembranes.In: Current Topics in Bioenergetics. D.R. Sanadi, editor. Vol. 1, p. 1. Academic Press, New YorkGoogle Scholar
  39. Williamson, R.L., Metcalf, R.L. 1967. Salicylanilides: A new group of active uncouplers of oxidative phosphorylation.Science 158:1694PubMedGoogle Scholar
  40. Yamaguchi, A., Anraku, Y. 1978. Mechanism of 3,5-di-tert-butyl-4-hydroxybenzylidene-malononitrile-mediated proton uptake in liposomes: Kinetics of proton uptake compensated by valinomycin-induced K+-efflux.Biochim. Biophys. Acta 501:136PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1981

Authors and Affiliations

  • Jos C. Arents
    • 1
  • Klaas J. Hellingwerf
    • 1
  • Karel van Dam
    • 1
  • Hans V. Westerhoff
    • 1
  1. 1.Laboratory of Biochemistry, B.C.P. Jansen InstituteUniversity of AmsterdamAmsterdamThe Netherlands

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