Abstract
When purple-membrane fragments from Halobacterium halobium are added to one aqueous phase of a positively-charged black lipid membrane, the membrane becomes photoelectrically active. Under normal conditions the steady-state photo-current is extremely low, but increases considerably when the lipid bilayer is doped with proton-permeable gramicidin channels or with a lipophilic acid-base system. These findings indicate that the purple-membrane sheets are bound to the surface of the bilayer, forming a sandwich-like structure. The time-behaviour of the photocurrent may be interpreted on the basis of a simple equivalent circuit which contains the conductance and capacitance of the purple membrane in series with the conductance and capacitance of the lipid bilayer. From the dependence of the photocurrent on the polarization of the exciting light the average angle between the transition moment of the retinal chromophore and the plane of the bilayer was calculated to be about 28 degrees. Furthermore, it was shown that chromophore-free apomembrane binds to the lipid bilayer and that its photoelectrical activity can be restored in situ by adding all-trans-retinal to the aqueous phase.
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Bamberg, B., Alpes, H., Apell, H.-J., Benz, R., Janko, K., Kolb, H.-A., Läuger, P., Gross, E.: Studies on the gramicidin channel. In: Biochemistry of Membrane Transport. FEBS Symposium, No. 42. G. Semenza and E. Carafoli (eds.), pp. 179–201. Berlin, Heidelberg, New York: Springer 1977
Becher, B., Ebrey, T. G.: The quantum efficiency of the photochemical conversion of the purple membrane protein. Biophys. J.17, 185–191 (1977)
Becher, B., Cassim, J. V.: Effects of bleaching and regeneration of the purple membrane structure of Halobacterium halobium. Biophys. J.19, 285–297 (1977)
Blok, M. C., Hellingwerf, K. I., Van Dam, K.: Reconstitution of bacteriorhodopsin in a millipore filter system. FEBS Lett.76, 45–50 (1977)
Blok, M. C., Van Dam, K.: Association of bacteriorhodopsin-containing phospholipid vesicles with phospholipid-impregnated millipore filters. Biochim. Biophys. Acta507, 48–61 (1978)
Bogomolni, R. A., Hwang, S.-B., Tseng, V.-W., King, G. I., Stoeckenius, W.: Orientation of the bacteriorhodopsin transition dipole. Biophys. J.17, 98a, Abstr. W-POS-C13 (1977)
Campion, A., El-Sayed, M. A., Terner, J.: Resonance raman kinetic spectroscopy of bacteriorhodopsin on the microsecond time scale. Biophys. J.20, 369–375 (1977)
Cohen, F. S., Eisenberg, M., McLaughlin, S.: The kinetic mechanism of action of an uncoupler of oxidative phosphorylation. J. Membr. Biol. (1978)
Criddle, R. S., Packer, L., Shieh, P.: Oligomycin-dependent ionophoric protein subunit of mitochondrial adenosin triphosphatase. Proc. Natl. Acad. Sci. USA74, 4306–4310 (1977)
Dancsházy, Z., Karvaly, B.: Incorporation of bacteriorhodopsin into a bilayer lipid membrane; a photoelectric-spectroscopic study. FEBS Lett.72, 136–138 (1976)
Dencher, N., Wilms, M.: Flash photometric experiments on the photochemical cycle of bacteriorhodopsin. Biophys. Struct. Mech.1, 259–271 (1975)
Drachev, L. A., Jasaitis, A. A., Kaulen, A. D., Kondrashin, A. A., Liberman, E. A., Nemecek, I. B., Ostroumov, S. A., Semenov, A. Yu., Skulachev, V. P.: Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature249, 321–324 (1974)
Drachev, L. A., Frolov, V. N., Kaulen, A. D., Liberman, E. A., Ostroumov, S. A., Plakunova, V. G., Semenov, A. Yu., Skulachev, V. P.: Reconstitution of biological molecular generators of electric current. J. Biol. Chem.251, 7059–7065 (1976)
Drachev, L. A., Kaulen, A. D., Skulachev, V. P.: Time resolution of the intermediate steps in the bacteriorhodopsin-linked electrogenesis. FEBS Lett.87, 161–167 (1978)
Fisher, K. A., Yanagimoto, K., Stoeckenius, W.: Oriented adsorption of purple membrane to cationic surfaces. J. Cell Biol.77, 611–621 (1978)
Frehland, E.: Dynamical theory of fluorescence polarization in a planar array of oriented pigment molecules. Biophys. Chem.4, 65–78 (1976)
Goldschmidt, C. R., Kalisky, O., Rosenfeld, T., Ottolenghi, M.: The quantum efficiency of the bacteriorhodopsin photocycle. Biophys. J.17, 179–183 (1977)
Henderson, R.: The structure of the purple membrane from Halobacterium halobium: Analysis of the X-ray diffraction pattern. J. Mol. Biol.93, 123–138 (1975)
Henderson, R.: The purple membrane from Halobacterium halobium. Annu. Rev. Biophys. Bioeng.6, 87–109 (1977)
Herrmann, T. R., Rayfield, G. W.: A measurement of the proton current generated by bacteriorhodopsin in black lipid membranes. Biochim. Biophys. Acta443, 623–628 (1976)
Herrmann, T. R., Rayfield, G. W.: The electrical response to light of bacteriorhodopsin in planar membranes. Biophys. J.21, 111–125 (1978)
Heyn, M. P., Cherry, R. J., Müller, U.: Transient and linear dichroism studies on bacteriorhodopsin: Determination of the orientation of the 568 nm all-trans retinal chromophore. J. Mol. Biol.117, 607–620 (1977)
Hirsch, M. D., Marcus, M. A., Lewis, A., Mahr, H., Figo, N.: A method for measuring picosecond phenomena in photolabile species. The emission lifetime of bacteriorhodopsin. Biophys. J.16, 1399–1409 (1976)
Hladky, S. B., Haydon, D. A.: Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel. Biochim. Biophys. Acta274, 294–312 (1972)
Hwang, S.-B., Korenbrot, J. I., Stoeckenius, W.: Proton transport by bacteriorhodopsin through an interface film. J. Membr. Biol.36, 137–158 (1977)
Janko, K., Benz, R.: Properties of lipid bilayer membranes made from lipids containing phytanic acid. Biochim. Biophys. Acta470, 8–16 (1977)
Karvaly, B., Dancsházy, Z.: Bacteriorhodopsin: a molecular photoelectric regulator. Quenching of photovoltaic effect on BLM containing bacteriorhodopsin. FEBS Lett.76, 36–40 (1977)
Kaufmann, K. J., Renzepis, P. M., Stoeckenius, W., Lewis, A.: Primary photochemical processes in bacteriorhodopsin. Biochem. Biophys. Res. Commun.68, 1109–1115 (1976)
Korenstein, R., Hess, B.: Immobilization of bacteriorhodopsin and orientation of its transition moment in purple membrane. FEBS Lett.89, 15–20 (1978)
Kung, M. C., DeVault, D., Hess, B., Oesterhelt, D.: Photolysis of bacterial rhodopsin. Biophys. J.15, 907–911 (1975)
Läuger, P., Lesslauer, W., Marti, E., Richter, J.: Electrical properties of bimolecular phospholipid membranes. Biochim. Biophys. Acta135, 20–32 (1967)
LeBlanc, O. H., Jr.: The effect of uncouplers of oxidative phosphorylation on lipid bilayer membranes: Carbonylcyanide-m-chlorophenylhydrazone. J. Membr. Biol.4, 227–251 (1971)
Lewis, A., Spoonhower, J., Bogomolni, R. A., Lozier, R. H., Stoeckenius, W.: Tunable Laser resonance Raman spectroscopy of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA71, 4462–4466 (1974)
Lozier, R. H., Bogomolni, R. A., Stoeckenius, W.: Bacteriorhodopsin, a light-driven proton pump in Halobacterium halobium. Biophys. J.15, 955–962 (1975)
Lozier, R. H., Niederberger, W., Bogomolni, R. A., Hwang, S.-B., Stoeckenius, W.: Kinetics and stoichiometry of light-induced proton release and uptake from purple membrane fragments, Halobacterium halobium cell envelopes, and phospholipid vesicles containing oriented pruple membranes. Biochim. Biophys. Acta440, 545–556 (1976)
Marcus, M. A., Lewis, A.: Kinetic resonance raman spectroscopy: Dynamics of deprotonation of the Schiff base of bacteriorhodopsin. Science195, 1328–1330 (1977)
Oesterhelt, D., Stoeckenius, W.: Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature [New Biol.]233, 149–152 (1971)
Oesterhelt, D., Meentzen, M., Schuhmann, L.: Reversible dissociation of the purple complex in bacteriorhodopsin and identification of 13-cis and all-trans-retinal as its chromophores. Eur. J. Biochem.40, 453–463 (1973)
Oesterhelt, D., Stoeckenius, W.: Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA70, 2853–2857 (1973)
Oesterhelt, D., Hess, B.: Reversible photolysis of the purple complex in the purple membrane of Halobacterium halobium. Eur. J. Biochem.37, 316–326 (1973)
Oesterhelt, D., Schuhmann, L., Gruber, H.: Light-dependent reaction of bacteriorhodopsin with hydroxylamine in cell suspensions of Halobacterium halobium: Demonstration of an apomembrane. FEBS Lett.44, 257–261 (1974)
Oesterhelt, D.: Isoprenoids and bacteriorhodopsin in Halobacteria. Prog. Mol. Subcell. Biol.4, 133–166 (1976)
Packer, L., Konishi, T., Shieh, P.: Conformational changes in bacteriorhodopsin accompanying ionophore activity. Fed. Proc.36, 1819–1823 (1977)
Renthal, R.: Apparent pK of photolabile proton binding in bacteriorhodopsin. Biochem. Biophys. Res. Commun.77, 155–161 (1977)
Sherman, W. V., Slifkin, M. A., Caplan, S. R.: Kinetic studies of phototransients in bacteriorhodopsin. Biochim. Biophys. Acta423, 238–248 (1976)
Shieh, P., Packer, L.: Photo-induced potentials across a polymer stabilized planar membrane in the presence of bacteriorhodopsin. Biochem. Biophys. Res. Commun.71, 603–609 (1976)
Sperling, W., Carl, P., Rafferty, Ch. N., Dencher, N. A.: Photochemistry and dark equilibrium of retinal isomers and bacteriorhodopsin isomers. Biophys. Struct. Mech.3, 79–94 (1977)
Steinemann, A., Stark, G., Läuger, P.: Orientation of the porphyrin ring in artificial chlorophyll membranes. J. Membr. Biol.9, 177–194 (1972)
Trissl, H.-W., Montal, M.: Electrical demonstration of rapid light-induced conformational changes in bacteriorhodopsin. Nature266, 655–657 (1977)
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Bamberg, E., Apell, H.J., Dencher, N.A. et al. Photocurrents generated by bacteriorhodopsin on planar bilayer membranes. Biophys. Struct. Mechanism 5, 277–292 (1979). https://doi.org/10.1007/BF02426663
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DOI: https://doi.org/10.1007/BF02426663