Skip to main content

Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion

Biochemistry (Moscow) volume 70, pages 251–256 (2005)Cite this article

Abstract

Proton transfer between water and the interior of membrane proteins plays a key role in bioenergetics. Here we survey the mechanism of this transfer as inferred from experiments with flash-triggered enzymes capturing or ejecting protons at the membrane surface. These experiments have revealed that proton exchange between the membrane surface and the bulk water phase proceeds at ≥1 msec because of a kinetic barrier for electrically charged species. From the data analysis, the barrier height for protons could be estimated as about 0.12 eV, i.e., high enough to account for the observed retardation in proton exchange. Due to this retardation, the proton activity at the membrane surface might deviate, under steady turnover of proton pumps, from that measured in the adjoining water phase, so that the driving force for ATP synthesis might be higher than inferred from the bulk-to-bulk measurements. This is particularly relevant for alkaliphilic bacteria. The proton diffusion along the membrane surface, on the other hand, is unconstrained and fast, occurring between the neighboring enzymes at less than 1 µsec. The anisotropy of proton dynamics at the membrane surface helps prokaryotes diminish the “futile” escape of pumped protons into the external volume. In some bacteria, the inner membrane is invaginated, so that the “ejected ” pro tons get trapped in the closed space of such intracellular membrane “sacks” which can be round or flat. The chloroplast thylakoids and the mitochondrial cristae have their origin in these intracellular structures.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

REFERENCES

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

    PubMed  CAS  Google Scholar 

  2. Mitchell, P. (1966) Physiol. Rev., 41, 445–502.

    CAS  Google Scholar 

  3. Skulachev, V. P. (1977) FEBS Lett., 74, 1–9.

    PubMed  CAS  Google Scholar 

  4. Skulachev, V. P. (1992) Eur. J. Biochem., 208, 203–209.

    PubMed  CAS  Google Scholar 

  5. Williams, R. J. P. (1978) Biochim. Biophys. Acta, 505, 1–44.

    PubMed  CAS  Google Scholar 

  6. Krulwich, T. A., Ito, M., Gilmour, R., Sturr, M. G., Guffanti, A. A., and Hicks, D. B. (1996) Biochim. Biophys. Acta, 1275, 21–26.

    PubMed  Google Scholar 

  7. Guffanti, A. A., Mann, M., Sherman, T. L., and Krulwich, T. A. (1984) J. Bacteriol., 159, 448–452.

    PubMed  CAS  Google Scholar 

  8. Ferguson, S. J. (1985) Biochim. Biophys. Acta, 811, 47–95.

    CAS  Google Scholar 

  9. Cramer, W. A., and Knaff, D. B. (1991) Energy Transduction in Biological Membranes: a Textbook of Bioenergetics, Springer, New York.

    Google Scholar 

  10. Ferguson, S. J. (1995) Curr. Biol., 5, 25–27.

    PubMed  CAS  Google Scholar 

  11. Kell, D. B. (1979) Biochim. Biophys. Acta, 549, 55–99.

    PubMed  CAS  Google Scholar 

  12. Michel, H., and Oesterhelt, D. (1980) Biochemistry, 19, 4615–4619.

    PubMed  CAS  Google Scholar 

  13. Guffanti, A. A., and Krulwich, T. A. (1984) Biochem. Soc. Trans., 12, 411–412.

    PubMed  CAS  Google Scholar 

  14. Kell, D. B. (1986) Meth. Enzymol., 127, 538–557.

    Article  PubMed  CAS  Google Scholar 

  15. Eigen, M. (1963) Angew. Chem., 75, 489–588.

    CAS  Google Scholar 

  16. Wraight, C. A., Cogdell, R. J., and Chance, B. (1978) in The Photosynthetic Bacteria (Clayton, R. K., and Sistrom, W. R., eds.) Academic Press, New York, pp. 471–511.

    Google Scholar 

  17. Junge, W., and Jackson, J. B. (1982) in Photosynthesis (Govindjee, ed.) Vol. 1, Academic Press, New York, pp. 589–646.

    Google Scholar 

  18. Chance, B., Crofts, A. R., Nishimura, M., and Price, B. (1970) Eur. J. Biochem., 13, 364–374.

    PubMed  CAS  Google Scholar 

  19. Codgell, R. J., Jackson, J. B., and Crofts, A. R. (1972) Bioenerg., 4, 413–429.

    Google Scholar 

  20. Petty, K. M., and Dutton, P. L. (1976) Arch. Biochem. Biophys., 172, 335–345.

    PubMed  CAS  Google Scholar 

  21. Auslander, W., and Junge, W. (1974) Biochim. Biophys. Acta, 357, 285–298.

    PubMed  CAS  Google Scholar 

  22. Drachev, A. L., Kaulen, A. D., and Skulachev, V. P. (1984) FEBS Lett., 178, 331–336.

    CAS  Google Scholar 

  23. Heberle, J., and Dencher, N. A. (1990) FEBS Lett., 277, 277–280.

    PubMed  CAS  Google Scholar 

  24. Heberle, J., and Dencher, N. A. (1992) Proc. Natl. Acad. Sci. USA, 89, 5996–6000.

    PubMed  CAS  Google Scholar 

  25. Heberle, J., Riesle, J., Thiedemann, G., Oesterhelt, D., and Dencher, N. A. (1994) Nature, 370, 379–382.

    PubMed  CAS  Google Scholar 

  26. Scherrer, P., Alexiev, U., Marti, T., Khorana, H. G., and Heyn, M. P. (1994) Biochemistry, 33, 13684–13692.

    PubMed  CAS  Google Scholar 

  27. Dioumaev, A. K., Richter, H. T., Brown, L. S., Tanio, M., Tuzi, S., Saito, H., Kimura, Y., Needleman, R., and Lanyi, J. K. (1998) Biochemistry, 37, 2496–2506.

    PubMed  CAS  Google Scholar 

  28. Porschke, D. (2002) J. Phys. Chem. B, 106, 10233–10241.

    CAS  Google Scholar 

  29. Gopta, O. A., Cherepanov, D. A., Junge, W., and Mulkidjanian, A. Y. (1999) Proc. Natl. Acad. Sci. USA, 96, 13159–13164.

    PubMed  CAS  Google Scholar 

  30. Junge, W., and Polle, A. (1986) Biochim. Biophys. Acta, 848, 265–273.

    CAS  Google Scholar 

  31. Heberle, J., and Dencher, N. A. (1992) in Structures and Functions of Retinal Proteins (Rigaud, J. L., ed.) John Libbey Eurotext Ltd, pp. 221–224.

  32. Junge, W., and McLaughlin, S. (1987) Biochim. Biophys. Acta, 890, 1–5.

    PubMed  CAS  Google Scholar 

  33. Jones, M. R., and Jackson, J. B. (1989) Biochim. Biophys. Acta, 975, 34–43.

    CAS  Google Scholar 

  34. Nachliel, E., and Gutman, M. (1996) FEBS Lett., 393, 221–225.

    PubMed  CAS  Google Scholar 

  35. Georgievskii, Y., Medvedev, E. S., and Stuchebrukhov, A. A. (2002) Biophys. J., 82, 2833–2846.

    PubMed  CAS  Google Scholar 

  36. Riesle, J., Oesterhelt, D., Dencher, N. A., and Heberle, J. (1996) Biochemistry, 35, 6635–6643.

    PubMed  CAS  Google Scholar 

  37. Adelroth, P., and Brzezinski, P. (2004) Biochim. Biophys. Acta, 1655, 102–115.

    PubMed  CAS  Google Scholar 

  38. Cherepanov, D. A., Junge, W., and Mulkidjanian, A. Y. (2004) Biophys. J., 86, 665–680.

    PubMed  CAS  Google Scholar 

  39. Heberle, J. (1991) Zeitauflosende Untersuchung der Protonentranslokationsschritte von bakteriorhodopsin mittels chemisch-gekoppelter pH-Indikatoren, PhD Thesis, Freien Universitat, Berlin.

    Google Scholar 

  40. Cherepanov, D. A., Feniouk, B. A., Junge, W., and Mulkidjanian, A. Y. (2003) Biophys. J., 85, 1307–1316.

    PubMed  CAS  Google Scholar 

  41. Cherepanov, D. A. (2005) Phys. Rev. Lett., in press.

  42. Maroti, P., and Wraight, C. A. (1997) Biophys. J., 73, 367–381.

    PubMed  CAS  Google Scholar 

  43. Arata, H., Takenaka, I., and Nishimura, M. (1987) J. Biochem., 101, 261–265.

    PubMed  CAS  Google Scholar 

  44. Jones, M. R., and Jackson, J. B. (1990) Biochim. Biophys. Acta, 1019, 51–58.

    CAS  Google Scholar 

  45. Mulkidjanian, A. Y., and Junge, W. (1994) FEBS Lett., 353, 189–193.

    PubMed  CAS  Google Scholar 

  46. Kramer, D. M., Sacksteder, C. A., and Cruz, J. A. (1999) Photosynth. Res., 60, 151–163.

    CAS  Google Scholar 

  47. Skulachev, V. P. (2001) Trends Biochem. Sci., 26, 23–29.

    PubMed  CAS  Google Scholar 

  48. Heberle, J. (2000) Biochim. Biophys. Acta, 1458, 135–147.

    PubMed  CAS  Google Scholar 

  49. Alexiev, U., Mollaaghababa, R., Scherrer, P., Khorana, H. G., and Heyn, M. P. (1995) Proc. Natl. Acad. Sci. USA, 92, 372–376.

    PubMed  CAS  Google Scholar 

  50. Serowy, S., Saparov, S. M., Antonenko, Y. N., Kozlovsky, W., Hagen, V., and Pohl, P. (2003) Biophys. J., 84, 1031–1037.

    PubMed  CAS  Article  Google Scholar 

  51. Amchenkova, A. A., Bakeeva, L. E., Chentsov, Y. S., Skulachev, V. P., and Zorov, D. B. (1988) J. Cell Biol., 107, 481–495.

    PubMed  CAS  Google Scholar 

  52. Severina, I. I., Skulachev, V. P., and Zorov, D. B. (1988) J. Cell Biol., 107, 497–501.

    PubMed  CAS  Google Scholar 

  53. Feniouk, B. A., Kozlova, M. A., Knorre, D. A., Cherepanov, D. A., Mulkidjanian, A. Y., and Junge, W. (2004) Biophys. J., 86, 4094–4109.

    PubMed  CAS  Google Scholar 

  54. Cherepanov, D. A., Mulkidjanian, A. Y., and Junge, W. (1999) FEBS Lett., 449, 1–6.

    PubMed  CAS  Google Scholar 

  55. Andersson, S. G. E., Zomorodipour, A., Andersson, J. O., Sicheritz-Ponten, T., Alsmark, U. C. M., Podowski, R. M., Naslund, A. K., Eriksson, A. S., Winkler, H. H., and Kurland, C. G. (1998) Nature, 396, 133–140.

    PubMed  CAS  Google Scholar 

  56. Kozlova, M. V., Gramadskii, K. B., Solodovnikova, I. M., Krasinskaya, I. P., Vinogradov, A. V., and Yaguzhinskii, L. S. (2003) Biofizika, 48, 443–452.

    PubMed  CAS  Google Scholar 

  57. Solodovnikova, I. M., Yurkov, V. I., Ton’shin, A. A., and Yaguzhinskii, L. S. (2004) Biofizika, 49, 47–56.

    PubMed  CAS  Google Scholar 

  58. Mitchell, P. (1991) Biosci. Rep., 11, 297–344.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Biophysics, Department of Biology/Chemistry, University of Osnabrück, D-49069, Osnabrück, Germany

    A. Y. Mulkidjanian & W. Junge

  2. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119899, Moscow, Russia

    A. Y. Mulkidjanian

  3. Institute of Electrochemistry, Russian Academy of Sciences, Leninsky pr. 31, 117071, Moscow, Russia

    D. A. Cherepanov

  4. Research Center Jülich, IBI-2: Structural Biology, D-52425, Jülich, Germany

    J. Heberle

Authors
  1. A. Y. Mulkidjanian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. A. Cherepanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Heberle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W. Junge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Y. Mulkidjanian.

Additional information

Translated from Biokhimiya, Vol. 70, No. 2, 2005, pp. 308–314.

Original Russian Text Copyright © 2005 by Mulkidjanian, Cherepanov, Heberle, Junge.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mulkidjanian, A.Y., Cherepanov, D.A., Heberle, J. et al. Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion. Biochemistry (Moscow) 70, 251–256 (2005). https://doi.org/10.1007/s10541-005-0108-1

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10541-005-0108-1

Key words

  • ATP synthesis
  • membrane potential
  • chemiosmotic coupling
  • alkaliphilic bacteria
  • chloroplasts
  • mitochondria
  • bacterial membranes