Skip to main content
SpringerLink
Log in

Proton migration along the membrane surface and retarded surface to bulk transfer

  • Letter
  • Published:

From Nature

View current issue Submit your manuscript

Abstract

SINCE the proposal of the chemiosmotic theory1 there has been a continuing debate about how protons that have been pumped across membranes reach another membrane protein that utilizes the established pH gradient. Evidence has been gathered in favour of a 'delocalized' theory, in which the pumped protons equilibrate with the aqueous bulk phase before being consumed, and a 'localized' one, in which protons move exclusively along the membrane surface2,3. We report here that after proton release by an integral membrane protein, long-range proton transfer along the membrane surface is faster than proton exchange with the bulk water phase. The rate of lateral proton diffusion can be calculated by considering the buffer capacity of the membrane surface. Our results suggest that protons can efficiently diffuse along the membrane surface between a source and a sink (for example H+-ATP synthase) without dissipation losses into the aqueous bulk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Mitchell, P. Nature 191, 144–148 (1961).

    Article  ADS  CAS  Google Scholar 

  2. Antonenko, Y. N., Kovbasnjuk, O. N. & Yaguzhinsky, L. S. Biochim. biophys. Acta 1150, 45–50 (1993).

    Article  CAS  Google Scholar 

  3. Prats, M., Teissié, J. & Tocanne, J.-F. Nature 322, 756–758 (1986).

    Article  ADS  CAS  Google Scholar 

  4. Michel, H. & Oesterhelt, D. Biochemistry 19, 4607–4614 (1980).

    Article  CAS  Google Scholar 

  5. Grzesiek, S. & Dencher, N. A. FEBS Lett. 208, 337–342 (1986).

    Article  CAS  Google Scholar 

  6. Heberle, J. & Dencher, N. A. Proc. natn. Acad. Sci. U.S.A. 89, 5996–6000 (1992).

    Article  ADS  CAS  Google Scholar 

  7. Heberle, J., Oesterhelt, D. & Dencher, N. A. EMBO J. 12, 3721–3727 (1993).

    Article  CAS  Google Scholar 

  8. Heberle, J. & Dencher, N. A. FEBS Lett. 277, 277–280 (1990).

    Article  CAS  Google Scholar 

  9. Grzesiek, S. & Dencher, N. A. Biophys. J. 50, 265–276 (1986).

    Article  ADS  CAS  Google Scholar 

  10. Burghaus, P. A. & Dencher, N. A. Archs Biochem. Biophys. 275, 395–409 (1989).

    Article  CAS  Google Scholar 

  11. Junge, W. & McLaughlin, S. Biochim. biophys. Acta 890, 1–5 (1987).

    Article  CAS  Google Scholar 

  12. Gutman, M. & Nachliel, E. Biochim. biophys. Acta 1015, 391–414 (1990).

    Article  CAS  Google Scholar 

  13. Oesterhelt, D. & Krippahl, G. FEBS Lett. 36, 72–76 (1973).

    Article  CAS  Google Scholar 

  14. Heberle, J. & Dencher, N. A. in Proton Transfer in Hydrogen-Bonded Systems (ed. Bountis, T.) 187–197 (Plenum, New York, 1992).

    Book  Google Scholar 

  15. Kasianowicz, J., Benz, R., Gutman, M. & McLaughlin, S. J. Membr. Biol. 99, 227 (1987).

    CAS  Google Scholar 

  16. Polle, A. & Junge, W. Biophys. J. 56, 27–31 (1989).

    Article  ADS  CAS  Google Scholar 

  17. Lechner, R. E., Dencher, N. A., Fitter, J., Büldt, G. & Belushkin, A. V. Biophys. Chem. 49, 91–99 (1994).

    Article  CAS  Google Scholar 

  18. Leberle, K., Kempf, I. & Zundel, G. Biophys. J. 55, 637–648 (1989).

    Article  ADS  CAS  Google Scholar 

  19. Schweiger, U., Tittor, J. & Oesterhelt, D. Biochemistry 33, 535–541 (1994).

    Article  CAS  Google Scholar 

  20. Flitsch, S. L. & Khorana, H. G. Biochemistry 28, 7800–7805 (1989).

    Article  CAS  Google Scholar 

  21. Bauer, P.-J., Dencher, N. A. & Heyn, M. P. Biophys. Struct. Mechanism 2, 79–92 (1976).

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Joachim Heberle

    Present address: Forschungszentrum Jülich, IBI-2, D-52425, Jülich, Germany

Authors and Affiliations

  1. Hahn-Meitner-lnstitut, NE, Glienicker Strasse 100, D-14109, Berlin, Germany

    Joachim Heberle

  2. MPI für Biochemie, Am Klopferspitz 18a, D-82152, Martinsried, Germany

    Jens Riesle, Gerd Thiedemann, Dieter Oesterhelt & Norbert A. Dencher

  3. TH Darmstadt, Institut für Biochemie, Petersenstrasse 22, D-64287, Darmstadt, Germany

    Norbert A. Dencher

Authors
  1. Joachim Heberle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jens Riesle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gerd Thiedemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dieter Oesterhelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Norbert A. Dencher
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heberle, J., Riesle, J., Thiedemann, G. et al. Proton migration along the membrane surface and retarded surface to bulk transfer. Nature 370, 379–382 (1994). https://doi.org/10.1038/370379a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/370379a0

  • Springer Nature Limited

This article is cited by

Search

Navigation