Electrical Double Layers in Pigment-Containing Biomembranes

  • Felix T. Hong
  • T. L. Okajima


Displacement photocurrents are unique to pigment-containing biomembranes. They belong to a special class of bioelectric signals that are generated by rapid charge displacements in the membranes. Interpretation of displacement photocurrents is not straightforward, and direct application of classical electrophysiological methodology is not adequate. However, a more comprehensive understanding of displacement photocurrents can be achieved by applying the Gouy-Chapman diffuse double layer theory to two possible prototype mechanisms of light-induced charge displacements. Macroscopically, a chemical capacitance in addition to the ordinary membrane capacitance must be invoked in the analysis of experimental data. By doing so, some apparent discrepancies of experimental observations can be readily resolved. In this paper, we use the bacteriorhodopsin membrane system to illustrate how the concept of chemical capacitance can assist experimentalists to achieve a meaningful decomposition of a multi-component displacement photocurrent signal. The general applicability of such an approach in other pigment-containing membrane systems of greater complexity is suggested.


Membrane Phase Planar Lipid Bilayer Purple Membrane Relaxation Time Constant Interfacial Charge Transfer 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andersen, O. S., Feldberg, S., Nakadomari, H., Levy, S., and McLaughlin, S., 1978, Electrostatic interactions among hydrophobic ions in lipid bilayer membranes, Biophys. J., 21:35–70.PubMedCrossRefGoogle Scholar
  2. Armstrong, C. M., and Bezanilla, F., 1974, Charge movement associated with the opening and closing of the activation gates of the Na channels, J. Gen. Physiol., 63:533–552.PubMedCrossRefGoogle Scholar
  3. Ballard, S. G., and Mauzerall, D. C., 1980, Photochemical ionogenesis in solutions of zinc octaethyl porphyrin, J. Chem. Phys., 72:933–947.CrossRefGoogle Scholar
  4. Bamberg, E., Fahr, A., and Szabo, G., 1984a, Photoelectric properties of the light-driven proton pump bacteriorhodopsin, in: “Electrogenic Transport: Fundamental Principles and Physiological Implications, Soc. Gen. Physiol. Ser., Vol. 38,” M. P. Blaustein and M. Lieberman, eds., Raven Press, New York, 381–394.Google Scholar
  5. Bamberg, E., Hegemann, P., and Oesterhelt, D., 1984b, Reconstitution of the light-driven electrogenic ion pump halorhodopsin in black lipid membranes, Biochim. Biophys. Acta, 773:53–60.CrossRefGoogle Scholar
  6. Bamberg, E., Hegemann, P., and Oesterhelt, D., 1984c, The chromoprotein of halorhodopsin is the light-driven electrogenic chloride pump in Halobacterium halobium. Biochem. (Wash.), 23:6216–6221.CrossRefGoogle Scholar
  7. Bamberg, E., Hegemann, P., and Oesterhelt, D., 1984d, Reconstitution of halorhodopsin in black lipid membranes, in: “Information and Energy Transduction in Biological Membranes,” C. L. Bolis, E. J. M. Helmreich, and H. Passow, eds., Alan R. Liss, Inc., New York, 73–79.Google Scholar
  8. Bayramashvili, D. I., Drachev, A. L., Drachev, L. A., Kaulen, A. D., Kudelin, A. B., Martynov, V. I., and Skulachev, V. P., 1984, Proteinase-treated photoreceptor discs: photoelectric activity of the partially-digested rhodopsin and membrane orientation, Eur. J. Biochem., 142:583–590.PubMedCrossRefGoogle Scholar
  9. Brown, K. T., and Murakami, M., 1964, A new receptor potential of the monkey retina with no detectable latency, Nature (London), 201:626–628.CrossRefGoogle Scholar
  10. Cafiso, D. S., and Hubbell, W. L., 1980, Light-induced interfacial potentials in photoreceptor membranes, Biophys. J., 30:243–264.PubMedCrossRefGoogle Scholar
  11. Carapellucci, P. A., and Mauzerall, D., 1975, Photosynthesis and porphyrin excited state redox reactions, Ann. N. Y. Acad. Sci., 244:214–238.PubMedCrossRefGoogle Scholar
  12. Chapron, Y., 1980, Rhodopsin-induced transient photopotentials in retinal and vesicle membranes, Photobiochem. Photobiophys., 1:297–304.Google Scholar
  13. Cone, R. A., and Pak, W . L., 1971, The early receptor potential, in: “Handbook of Sensory Physiology, Vol. I. Principles of Receptor Physiology,” W. R. Loewenstein, ed., Springer-Verlag, Berlin, 345–365.CrossRefGoogle Scholar
  14. Drachev, L. A., Kaulen, A. D., Ostroumov, S. A., and Skulachev, V. P., 1974, Electrogenesis by bacteriorhodopsin incorporated in a planar phospholipid membrane, FEBS Lett., 39:43–45.PubMedCrossRefGoogle Scholar
  15. Drachev, L. A., Frolov, V. N., Kaulen, A. D., Liberman, E. A., Ostroumov, S. A., Plakunova, V. G., Semenov, A. Yu., and Skulachev, V. P., 1976, Reconstitution of biological molecular generators of electric current: bacteriorhodopsin, J. Biol. Chem., 251:7059–7065.PubMedGoogle Scholar
  16. Drachev, L. A., Kaulen, A. D., and Skulachev, V. P., 1978, Time resolution of the intermediate steps in the bacteriorhodopsin-linked electrogenesis, FEBS Lett., 87:161–167.PubMedCrossRefGoogle Scholar
  17. Drachev, L. A., Kalamkarov, G. R., Kaulen, A. D., Ostrovsky, M. A., and Skulachev, V. P., 1980, Animal rhodopsin as a photogenerator of an electric potential that increases photoreceptor membrane permeability, FEBS Lett., 119:125–131.PubMedCrossRefGoogle Scholar
  18. Drachev, L. A., Kaulen, A. D., Khitrina, L. V., and Skulachev, V. P., 1981, Fast stages of photoelectric processes in biological membranes. I. bacteriorhodopsin, Eur. J. Biochem., 117:461–470.PubMedCrossRefGoogle Scholar
  19. Drachev, L. A., Kaulen, A. D., and Skulachev, V. P., 1984a, Correlation of photochemical cycle, H+ release and uptake, and electric events in bacteriorhodopsin. FEBS Lett., 178:331–335.CrossRefGoogle Scholar
  20. Drachev, L. A., Dracheva, S. M., Samuilov, V. D., Semenov, A. Yu., and Skulachev, V. P., 1984b, Photoelectric effects in bacterial chromato-phores: comparison on spectral and direct electrometric methods, Biochim. Biophys. Acta. 767:257–262.CrossRefGoogle Scholar
  21. Fahr, A., Lauger, P., and Bamberg, E., 1981, Photocurrent kinetics of purple-membrane sheets bound to planar bilayer membranes, J. Membrane Biol., 60:51–62.CrossRefGoogle Scholar
  22. Gräber, P., and Trissl, H.-W., 1981, On the rise time and polarity of the photovoltage generated by light gradients in chloroplast suspensions, FEBS Lett., 123:95–99.CrossRefGoogle Scholar
  23. Hagins, W. A., and Rüppel, H., 1971, Fast photoelectric effects and the properties of vertebrate photoreceptors as electric cables, Fed. Proc. 30:64–68.PubMedGoogle Scholar
  24. Hong, F .T., 1976, Charge transfer across pigmented bilayer lipid membrane and its interfaces, Photochem. Photobiol., 24:155–189.PubMedCrossRefGoogle Scholar
  25. Hong, F. T., 1977, Photoelectric and magneto-orientation effects in pigmented biological membranes, J. Colloid Interface Sci., 58:471–497.CrossRefGoogle Scholar
  26. Hong, F. T., 1978, Mechanisms of generation of the early receptor potential revisited. Bioelectrochem. Bioenerg., 5:425–455.CrossRefGoogle Scholar
  27. Hong, F. T., 1980, Displacement photocurrents in pigment-containing biomembranes: artificial and natural systems, in: “Bioelectrochemistry: Ions, Surfaces, Membranes, ACS Advances in Chemistry Ser., Vol. 188,” M. Blank, ed., American Chemical Society, Washington, D.C., 211–237.CrossRefGoogle Scholar
  28. Hong, F. T., and Mauzerall, D., 1974, Interfacial photoreactions and chemical capacitance in lipid bilayers, Proc. Natl. Acad. Sci. USA. 71:1564–1568.PubMedCrossRefGoogle Scholar
  29. Hong, F. T., and Mauzerall, D., 1976, Tunable voltage clamp method: application to photoelectric effects in pigmented bilayer lipid membranes, J. Electrochem. Soc., 123:1317–1324.CrossRefGoogle Scholar
  30. Hong, F. T., and Montai, M., 1979, Bacteriorhodopsin in model membranes: a new component of the displacement photocurrent in the microsecond time scale. Biophys. J., 25:465–472.PubMedCrossRefGoogle Scholar
  31. Huebner, J. S., Arrieta, R. T., Arrieta, I. C., and Pachori, P. M., 1984, Photo-electric effects in bilayer membranes; electrometers and voltage clamps compared, Photochem. Photobiol., 39:191–198.CrossRefGoogle Scholar
  32. Keszthelyi, L., 1984, Intramolecular charge shifts during the photoreaction cycle of bacteriorhodopsin, in: “Information and Energy Transduction in Biological Membranes,” C. L. Bolis, E. J. M. Helmreich, and H. Passow, eds., Alan R. Liss, Inc., New York, 51–71.Google Scholar
  33. Keszthelyi, L., and Ormos, P., 1980, Electric signals associated with the photocycle of bacteriorhodopsin, FEBS Lett., 109:189–193.CrossRefGoogle Scholar
  34. Losev, A., and Mauzerall, D., 1983, Photoelectron transfer between a charged derivative of chlorophyll and ferricyanide at the lipid bilayer-water interface. Photochem. Photobiol., 38:355–361.CrossRefGoogle Scholar
  35. Mauzerall, D., 1979, Photoinduced electron transfer at the water-lipid bilayer interface, in: “Light-Induced Charge Separation in Biology and Chemistry,” H. Gerischer and J. J. Katz, eds., Verlag Chemie GmbH, Weinheim, 241–257.Google Scholar
  36. Mauzerall, D., and Hong, F. T., 1975, Photochemistry of porphyrins in membranes and photosynthesis, in: “Porphyrins and Metalloporphyrins,” K. M. Smith, ed., Elsevier, Amsterdam, 701–725.Google Scholar
  37. Mueller, P., Rudin, D. O., Tien, H. T., and Wescott, W. C., 1962, Reconstitution of excitable cell membrane structure in vitro. Circulation. 26:1167–1171.Google Scholar
  38. Okajima, T. L., and Hong, F. T., 1985, Kinetic analysis of displacement photocurrents elicited in two types of bacteriorhodopsin model membranes, manuscript submitted to Biophysical Journal.Google Scholar
  39. Packham, N. K., Dutton, P. L., and P. Mueller, 1982, Photoelectric currents across planar bilayer membranes containing bacterial reaction centers: response under conditions of single electron turnover, Biophys. J., 37:465–473.PubMedCrossRefGoogle Scholar
  40. Rayfield, G. W., 1983, Events in proton pumping by bacteriorhodopsin, Biophys. J., 41:109–117.PubMedCrossRefGoogle Scholar
  41. Schönfeld, M., Montai, M., and G. Feher, 1979, Functional reconstitution of photosynthetic reaction centers in planar lipid bilayers, Proc. Natl. Acad. Sci. USA. 76:6351–6355.PubMedCrossRefGoogle Scholar
  42. Skulachev, V. P., 1982, A single turnover study of photoelectric current-generating proteins, Methods Enzvmol., 88:35–45.CrossRefGoogle Scholar
  43. Smith, S. O., Myers, A. B., Pardoen, J. A., Winkel, C., Mulder, P. P. J., Lugtenburg, J., and Mathies, R., 1984, Determination of retinal Schiff base configuration in bacteriorhodopsin, Proc. Natl. Acad. Sci. USA. 81:2055–2059.PubMedCrossRefGoogle Scholar
  44. Stoeckenius, W., and Bogomolni, R. A., 1982, Bacteriorhodopsin and related pigments of Halobacteria. Ann. Rev. Biochem., 51:587–616.PubMedCrossRefGoogle Scholar
  45. Tien, H. T., 1968, Light-induced phenomena in black lipid membranes constituted from photosynthetic pigments, Nature (London). 219:272–274.CrossRefGoogle Scholar
  46. Tien, H. T., 1974, “Bilayer Lipid Membranes (BLM): theory and practice,” Marcel Dekker, New York, 245–321.Google Scholar
  47. Trissl, H.-W., 1979, Light-induced conformational changes in cattle rhodopsin as probed by measurements of the interface potential, Photochem. Photobiol., 29:579–588.PubMedCrossRefGoogle Scholar
  48. Trissl, H.-W., 1980, I. Novel capacitative electrode with a wide frequency range for measurements of flash-induced changes of interface potential at the oil-water interface, Biochim. Biophys. Acta. 595:82–95.PubMedCrossRefGoogle Scholar
  49. Trissl, H.-W., 1981, The concept of chemical capacitance: a critique, Biophys. J., 33:233–242.PubMedCrossRefGoogle Scholar
  50. Trissl, H.-W., 1982, Electrical responses to light: fast photovoltages of rhodopsin-containing membrane systems and their correlation with the spectral intermediates, Methods Enzymol., 81:431–439.PubMedCrossRefGoogle Scholar
  51. Trissl, H.-W., 1983a, Charge displacements in purple membranes adsorbed to a heptane/water interface: evidence for a primary charge separation in bacteriorhodopsin, Biochim. Biophys. Acta. 723:327–331.CrossRefGoogle Scholar
  52. Trissl, H.-W., 1983b, Spatial correlation between primary redox components in reaction centers of Rhodopseudomonas sphaeroides measured by two electrical methods in the nanosecond range, Proc. Natl. Acad. Sci. USA. 80:7173–7177.PubMedCrossRefGoogle Scholar
  53. Trissl, H.-W., 1985, I. Primary electrogenic processes in bacteriorhodopsin probed by photoelectric measurements with capacitative metal electrodes, Biochim. Biophys. Acta, 806:124–135.CrossRefGoogle Scholar
  54. Trissl, H.-W., and Graber, P., 1980a, II. Electrical measurements in the nanosecond range of the charge separation from chloroplasts spread at a heptane-water interface: application of a novel capacitative electrode, Biochim. Biophys. Acta. 595:96–108.PubMedCrossRefGoogle Scholar
  55. Trissl, H.-W., and Gräber, P., 1980b, Properties of chloroplasts spread at the heptane/water interface: measurements of the photo synthetic charge separation in the nanosecond range, Bioelectrochem. Bioenerg., 7:167–186.CrossRefGoogle Scholar
  56. Trissl, H.-W., and Kunze, U., 1985, II. Primary electrogenic reactions in chloroplasts probed by picosecond flash-induced dielectric polarization, Biochim. Biophys. Acta. 806:136–144.CrossRefGoogle Scholar
  57. Trissl, H.-W., and Montai, M., 1977, Electrical demonstration of rapid light-induced conformational changes in bacteriorhodopsin, Nature (London). 266:655–657.CrossRefGoogle Scholar
  58. Trissl, H.-W., Kunze, Ü., and Junge, W., 1982, Extremely fast photoelectric signals from suspensions of broken chloroplasts and of isolated chromatophores, Biochim. Biophys. Acta. 682:364–377.CrossRefGoogle Scholar
  59. Trissl, H.-W., Der, A., Ormos, P., and Keszthelyi, L., 1984, Influence of stray capacitance and sample resistance on the kinetics of fast photo-voltages from oriented purple membranes, Biochim. Biophys. Acta. 765:288–294.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • Felix T. Hong
    • 1
  • T. L. Okajima
    • 1
  1. 1.Department of PhysiologyWayne State University School of MedicineDetroitUSA

Personalised recommendations