Advertisement

Proton Currents and Local Energy Coupling in Thylakoids: A Survey

  • Yaroslav de Kouchkovsky
  • Claude Sigalat
  • Francis Haraux
  • Suong Phung Nhu Hung

Summary

A survey of the experimental and conceptual basis of a microchemiosmotic interpretation of energy-dependent processes in thylakoids is presented. It assumes that protons circulate from their active transport points to their backflow ports in a heterogeneous medium, having a resistivity not only transversal, from membrane to isopotential bulk phase, but also lateral, in or on the membrane, an idea central to our hypothesis. Consequently, the proton electrochemical potential ΔμH at the H+-generators (redox carriers) is higher than ΔμH at H+-leaks (coupling factors and membrane pores), and the measured ΔμH is an average of local values. However, some flexibility in this microscopic coupling is possible, and a delocalized behaviour may sometimes be obtained by increasing the lumen volume (osmolarity decrease) and its conductivity (ionicity increase). A one-to-one link between primary and secondary pumps, as advocated by mosaic chemiosmosis, seems therefore improbable here.

The experimental procedure used in this investigation consisted in correlating electron flow, proton gradient (ΔpH, with or without Δψ), and phosphorylation rate in several conditions. To modulate ΔμH, H+ influx or efflux were adjusted by light or ionophore changes: contrary to the prediction of classical chemiosmosis, these two factors have no identical effects. Also, an increase of the distance between H+-translocators and coupling factors (SII chain vs. SI) lowers the phosphorylation efficiency of a given mean ΔμH, which is easily explained by a ΔμH drop along the lateral resistance mentioned above. Another approach was to compare redox control and phosphorylation in heavy water media, where proton circulation is hindered. Additional information given concerns possible occurrence of “scalar ATPases” and a quantitative estimate, at variable ΔpH, of proton flux across coupling factor, phosphorylating or not.

Keywords

Electron Flow Coupling Factor Proton Gradient Lumen Volume Strong Light 
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

ΔμH (\(\equiv \Delta \tilde{\mu }{{H}^{+}}\)), ΔpH, Δψ

differences in proton electrochemical potential, pH, and electric potential

with a bar on top

mean values, with superscripts E or C: local values, at electron-transfer chain and coupling-factor (CF)

subscripts e, i

external (stroma or medium) or internal (lumen) phases. SI, SII: systems I and II

Chl

chlorophyll, PQ: plastoquinone

DCPIP

2,6-dichlorophenolindophenol, DMQ: 2,5-dimethylquinone, FeCy: ferri-cyanide, MV: methylviologen, P: inorganic phosphate (Pi) or “high-energy” phosphate bond, PYO: pyocyanin, 9A: 9-aminoacridine. Ve-, VP: rates of electron flow and phosphorylation

RC

= redox control

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    P. Mitchell, Nature 191: 144–148 (1961).CrossRefGoogle Scholar
  2. 2.
    R. J. P. Williams, J. Theor. Biol. 1: 1–17 (1961).CrossRefGoogle Scholar
  3. 3.
    H. V. Westerhoff, B. A. Melandri, G. Venturoli, G. F. Azzone and D. B. Kell, FEBS Lett. 165: 1–5 (1984).CrossRefGoogle Scholar
  4. 4.
    Y. de Kouchkovsky and F. Haraux, Biochim. Biophys. Res. Commun. 99: 205–212 (1981).CrossRefGoogle Scholar
  5. 5.
    F. Haraux and Y. de Kouchkovsky, Physiol. Vég. 21: 563–576 (1983).Google Scholar
  6. 6.
    Y. de Kouchkovsky, F. Haraux and C. Sigalat, Bioelectrochem. Bioenerg. 13: 143–162 (1984).CrossRefGoogle Scholar
  7. 7.
    K. van Dam, A. H. C. A. Wiechmann, K. J. Hellingwerf, J. C. Arents and H. V. Westerhoff, in: “Membrane Proteins”, P. Nicholls, pp. 121–132, Pergamon Press, Oxford (1978).Google Scholar
  8. 8.
    F. Haraux and Y. de Kouchkovsky, Biochim. Biophys. Acta 679: 235–247 (1982).CrossRefGoogle Scholar
  9. 9.
    C. Sigalat, F. Haraux, F. de Kouchkovsky, S. Phung nhu Hung and Y. de Kouchkovsky, submitted to Biochim. Biophys. Acta.Google Scholar
  10. 10.
    G. Mackinney, J. Biol. Chem. 140: 315–322 (1941).Google Scholar
  11. 11.
    P. K. Glasoe and F. A. Long, J. Phys. Chem. 64: 188–190 (1960).CrossRefGoogle Scholar
  12. 12.
    M. Nishimura, T. Ito and B. Chance, Biochim. Biophys. Acta 59: 177–182 (1982).Google Scholar
  13. 13.
    J. L. Lemasters and C. R. Hackenbrock, in “Methods in Enzymology”, S. P. Colowick and N. 0. Kaplan, eds., 57, pp. 36–50, Acad. Press., New York (1978).Google Scholar
  14. 14.
    P. Gräber, U. Junesch and G. H. Schatz, Ber. Bunsenges. Phys. Chem. 88: 599–608 (1984).Google Scholar
  15. 15.
    S. Schuldiner, H. Rottenberg and M. Avron, Eur. J. Biochem. 25: 64–70 (1972).CrossRefGoogle Scholar
  16. 16.
    F. Haraux and Y. de Kouchkovsky, Biochim. Biophys. Acta 546: 455–471 (1979).CrossRefGoogle Scholar
  17. 17.
    A. H. C. M. Schapendonk and W. J. Vredenberg, Biochim. Biophys. Acta 462: 613–621 (1977).CrossRefGoogle Scholar
  18. 18.
    G. F. Azzone, T. Pozzan, S. Massari and M. Bragadin, Biochim. Biophys. Acta 501: 296–306 (1978).CrossRefGoogle Scholar
  19. 19.
    A. Baccarini-Melandri, R. Casadio and B. A. Melandri, Eur. J. Biochem. 78: 389–402 (1977).CrossRefGoogle Scholar
  20. 20.
    B. Andersson and W. Haehnel, FEBS Lett. 146: 13–17 (1982).CrossRefGoogle Scholar
  21. 21.
    F. Haraux, C. Sigalat, A. Moreau and Y. de Kouchkovsky, FEBS Lett. 155: 248–252 (1983).CrossRefGoogle Scholar
  22. 22.
    J. W. Davenport and R. E. McCarty, Biochim. Biophys. Acta 766: 363–374 (1984).CrossRefGoogle Scholar
  23. 23.
    J. Barber, Biochim. Biophys. Acta 594: 253–308 (1980).Google Scholar
  24. 24.
    A. B. Hope and D. B. Matthews, Aust. J. Plant Physiol. 12: 9–20 (1985).CrossRefGoogle Scholar
  25. 25.
    F. Haraux and Y. de Kouchkovsky, Biochim. Biophys. Acta 592: 153–168 (1980).CrossRefGoogle Scholar
  26. 26.
    Y. de Kouchkovsky, F. Haraux and C. Sigalat, FEBS Lett. 139: 245–249 (1982).CrossRefGoogle Scholar
  27. 27.
    U. Pick, H. Rottenberg and M. Avron, FEBS Lett. 32: 91–94 (1973).CrossRefGoogle Scholar
  28. 28.
    S. Izawa and N. E. Good, Biochim. Biophys. Acta 162: 380–391 (1968).CrossRefGoogle Scholar
  29. 29.
    M. Rathenow and B. Rumberg, Ber. Bunsenges. Phys. Chem. 84: 1059–1062 (1980).Google Scholar
  30. 30.
    M. Schönfeld and H. Schickler, FEES Lett. 167: 231–234 (1984).CrossRefGoogle Scholar
  31. 31.
    V. V. Lemeshko, Biofizika 27:420–424 (Engl. transi.: Biophysics 27: 429–434 (1982).Google Scholar
  32. 32.
    H. Woelders, W. J. van der Zande, A.-M. A. F. Colen, R. J. A. Wanders and K. van Dam, FEBS Lett. 179: 278–282 (1985).CrossRefGoogle Scholar
  33. 33.
    J. Duszynski and L. Wojtczak, FEBS Lett. 182: 243–248 (1985).CrossRefGoogle Scholar
  34. 34.
    E. Nachliel and M. Gutman, Eur. J. Bioch. 143: 83–88 (1984).CrossRefGoogle Scholar
  35. 35.
    J. Teissi4, M. Prats, P. Soucaille and J.-F. Tocanne, Proc. Natl. Acad. Sci. USA 82: 3217–3221 (1985).CrossRefGoogle Scholar
  36. 36.
    J. F. Nagle and H. J. Morowitz, Biophysics 75: 298–302 (1978).Google Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • Yaroslav de Kouchkovsky
    • 1
  • Claude Sigalat
    • 1
  • Francis Haraux
    • 1
  • Suong Phung Nhu Hung
    • 1
  1. 1.Laboratoire de PhotosynthèseC.N.R.S.Gif-sur-YvetteFrance

Personalised recommendations