Abstract
A description of the rate constants and the energetics of the elementary reaction steps of the photocycle of bacteriorhodopsin has been helpful in understanding the mechanism of proton transport in this light-driven pump. The evidence suggests a single unbranched reaction sequence, BR-hv → K ↔ L ↔ M1 → M2 ↔ O → BR, where coupling to the protonmotive force is at the energetically and mechanistically important M1 → M2 step. The consequences of site-specific mutations expressed homologously inHalobacterium halobium have revealed characteristics of the Schiff base deprotonation in the L → M1 reaction, the reorientation of the Schiff base from the extracellular to the cytoplasmic side in the M1 → M2 reaction, and the reprotonation of the Schiff base in the M2 → N reaction.
Similar content being viewed by others
References
Ames, J. B., and Mathies, R. A. (1990).Biochemistry 29, 7181–7190.
Aton, B., Doukas, A. G., Callender, R. H., Becher, B., and Ebrey, T. G. (1977).Biochemistry 16, 2995–2999.
Balashov, S. P., Govindjee, R., and Ebrey, T. G. (1991).Biophys. J. 60, 475–490.
Beach, J. M., and Fager, R. S. (1985).Photochem. Photobiol. 41, 557–562.
Birge, R. R. (1990).Biochim. Biophys. Acta 1016, 293–327.
Birge, R. R., and Cooper, T. M. (1983).Biophys. J. 42, 61–69.
Birge, R. R., Cooper, T. M., Lawrence, A. F., Masthay, M. B., Zhang, C.-F., and Zidovetzki, R. (1991).J. Am. Chem. Soc. 113, 4327–4328.
Bousché, O., Braiman, M., He, Y.-W., Marti, T., Khorana, H. G., and Rothschild, K. J. (1991).J. Biol. Chem. 266, 11063–11067.
Braiman, M. S., and Mathies, R. A. (1982).Proc. Natl. Acad. Sci. USA 79, 403–407.
Braiman, M. S., Mogi, T., Marti, T., Stern, L. J., Khorana, H. G., and Rothschild, K. J. (1988).Biochemistry 27, 8516–8520.
Braiman, M. S., Bousché, O., and Rothschild, K. J. (1991).Proc. Natl. Acad. Sci. USA 88, 2388–2392.
Cao, Y., Váró, G., Chang, M., Ni, B., Needleman, R., and Lanyi, J. K. (1991).Biochemistry 30, 10972–10979.
Dancsházy, Z., Helgerson, S. L., and Stoeckenius, W. (1983).Photobiochem. Photobiophys. 5, 347–357.
Dancsházy, Z., Govindjee, R., and Ebrey, T. G. (1988).Proc. Natl. Acad. Sci. USA 85, 6358–6361.
De Groot, H. J. M., Harbison, G. S., Herzfeld, J., and Griffin, R. G. (1989).Biochemistry 28, 3346–3353.
De Groot, H. J. M., Smith, S. O., Courtin, J., Van den Berg, E., Winkel, C., Lugtenburg, J., Griffin, R. G., and Herzfeld, J. (1990).Biochemistry 29, 6873–6883.
Drachev, L. A., Kaulen, A. D., and Skulachev, V. P. (1984).FEBS Lett. 178, 331–335.
Duñach, M., Marti, T., Khorana, H. G., and Rothschild, K. J. (1990).Proc. Natl. Acad. Sci. USA 87, 9873–9877.
Fischer, U., and Oesterhelt, D. (1979).Biophys. J. 28, 211–230.
Fodor, S. P., Ames, J. B., Gebhard, R., van der Berg, E. M., Stoeckenius, W., Lugtenburg, J., and Mathies, R. A. (1988).Biochemistry 27, 7097–7101.
Garty, H., Caplan, S. R., and Cahen, D. (1982).Biophys. J. 37, 405–415.
Gerwert, K., and Siebert, F. (1986).EMBO J. 5, 805–811.
Gerwert, K., Hess, B., Soppa, J., and Oesterhelt, D. (1989).Proc. Natl. Acad. Sci. USA 86, 4943–4947.
Gerwert, K., Hess, B., and Engelhard, M. (1990a).FEBS Lett. 261, 449–454.
Gerwert, K., Souvignier, G., and Hess, B. (1990b).Proc. Natl. Acad. Sci. USA 87, 9774–9778.
Groma, G. I., Helgerson, S. L., Wolber, P. K., Beece, D., Dancsházy, Z., Keszthelyi, L., and Stoeckenius, W. (1984).Biophys. J. 45, 985–992.
Grzesiek, S., and Dencher, N. A. (1986).FEBS Lett. 208, 337–342.
Hanamoto, J. H., Dupuis, P., and El-Sayed, M. A. (1984).Proc. Natl. Acad. Sci. USA 81, 7083–7087.
Harbison, G. S., Smith, S. O., Pardoen, J. A., Courtin, J., Lugtenburg, J., Herzfeld, J., Mathies, R. A., and Griffin, R. G. (1985).Biochemistry 24, 6955–6962.
Heberle, J., and Dencher, N. A. (1990).FEBS Lett. 277, 277–280.
Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E., and Downing, K. H. (1990).J. Mol. Biol. 213, 899–929.
Hofrichter, J., Henry, E. R., and Lozier, R. H. (1989).Biophys. J. 56, 693–706.
Kakitani, H., Kakitani, T., Rodman, H., and Honig, B. (1985).Photochem. Photobiol. 41, 471–479.
Kimura, Y., Ikegami, A., and Stoeckenius, W. (1984).Photochem. Photobiol. 40, 641–646.
Kobayashi, T., Ohtani, H., Iwai, J.-I., Ikegami, A., and Uchiki, H. (1983).FEBS Lett. 162, 197–200.
Koch, M. H. J., Dencher, N. A., Oesterhelt, D., Plöhn, H.-J., Rapp, G., and Büldt, G. (1991).EMBO J. 10, 521–526.
Kouyama, T., Nasuda-Kouyama, A., Ikegami, A., Mathew, M. K., and Stoeckenius, W. (1988).Biochemistry 27, 5855–5863.
Kouyama, T., and Nasuda-Kouyama, A. (1989).Biochemistry 28, 5963–5970.
Lanyi, J. K., Tittor, J., Váró, G., Krippahl, G., and Oesterhelt, D. (1992).Biochim. Biophys. Acta, in press.
Lozier, R. H., and Niederberger, W. (1977).Fed. Proc. 36, 1805–1809.
Lozier, R. H., Bogomolni, R. A., and Stoeckenius, W. (1975).Biophys. J. 15, 955–963.
Lozier, R. H., Niederberger, W., Ottolenghi, M., Sivorinovsky, G. and Stoeckenius, W. (1978). In:Energetics and Structure of Halophilic Microorganisms (Caplan, S. R., and Ginzburg, M., eds.), Elsevier/North Holland, Amsterdam, pp. 123–139.
Mathies, R. A., Lin, S. W., Ames, J. B., and Pollard, W. T. (1991).Annu. Rev. Biophys. Biophys. Chem. 20, 491–518.
Maurer, R., Vogel, J., and Schneider, S. (1987).Photochem. Photobiol. 46, 247–253.
Miercke, L. J. W., Betlach, M. C., Mitra, A. K., Shand, R. F., Fong, S. K., and Stroud, R. M. (1991).Biochemistry 30, 3088–3098.
Milder, S. J. (1991).Biophys. J. 60, 440–446.
Milder, S. J., Thorgeirsson, T. E., Miercke, L. J. W., Stroud, R. M., and Kliger, D. S. (1991).Biochemistry 30, 1751–1761.
Miller, A., and Oesterhelt, D. (1990).Biochim. Biophys. Acta 1020, 57–64.
Mogi, T., Stern, L. J., Marti, T., Chao, B. H., and Khorana, H. G. (1988).Proc. Natl. Acad. Sci. USA 85, 4148–4152.
Mowery, P. C., Lozier, R. H., Chae, Q., Tseng, Y. W., Taylor, M., and Stoeckenius, W. (1979).Biochemistry 18, 4100–4107.
Nagle, J. F., and Mille, M. (1981).J. Chem. Phys. 74, 1367–1372.
Nagle, J. F., Parodi, L. A., and Lozier, R. H. (1982).Biophys. J. 38, 161–174.
Nakanishi, K., Balogh-Nair, V., Arnaboldi, M., Tsujimoto, K., and Honig, B. (1980).J. Am. Chem. Soc. 102, 7945–7947.
Needleman, R., Chang, M., Ni, B., Váró, G., Fornes, J., White, S. H., and Lanyi, J. K. (1991).J. Biol. Chem. 266, 11478–11484.
Ormos, P. (1991).Proc. Natl. Acad. Sci. USA 88, 473–477.
Ort, D. R., and Parson, W. W. (1979a).Biophys. J. 25, 355–364.
Ort, D. R., and Parson, W. W. (1979b).Biophys. J. 25, 341–353.
Otto, H., Marti, T., Holz, M., Mogi, T., Lindau, M., Khorana, H. G., and Heyn, M. P. (1989).Proc. Natl. Acad. Sci. USA 86, 9228–9232.
Otto, H., Marti, T., Holz, M., Mogi, T., Stern, L. J., Engel, F., Khorana, H. G., and Heyn, M. P. (1990).Proc. Natl. Acad. Sci. USA 87, 1018–1022.
Pande, J., Callender, R. H., and Ebrey, T. G. (1981).Proc. Natl. Acad. Sci. USA 78, 7379–7382.
Pfefferlé, J.-M., Maeda, A., Sasaki, J., and Yoshizawa, T. (1991).Biochemistry 30, 6548–6556.
Renthal, R., Shuler, K. and Regalado, R. (1990).Biochim. Biophys. Acta 1016, 378–384.
Rothschild, K. J. (1992).J. Bioenerg. Biomembr. 24, 000–000.
Rothschild, K. J., Marrero, H., Braiman, M. S. and Mathies, R. A. (1984).Photochem. Photobiol. 40, 675–679.
Schulten, K., Schulten, Z., and Tavan, P. (1984). InInformation and Energy Transduction in Biological Membranes, (Bolis, A., Helmreich, H., and Passow, H., eds.), Alan R. Liss, Inc., New York, pp. 113–131.
Sherman, W. V., Slifkin, M. A., and Caplan, S. R. (1976).Biochim. Biophys. Acta 423, 238–248.
Sherman, W. V., Eicke, R. R., Stafford, S. R., and Wasacz, F. M. (1979).Photochem. Photobiol. 30, 727–729.
Shichida, Y., Matuoka, S., Hidaka, Y., and Yoshizawa, T. (1983).Biochim. Biophys. Acta 723, 240–246.
Smith, S. O., Pardoen, J. A., Mulder, P. P. J., Curry, B., Lugtenburg, J. and Mathies, R. A. (1983).Biochemistry 22, 6141–6148.
Smith, S. O., Lugtenburg, J., and Mathies, R. A. (1985).J. Membr. Biol. 85, 95–109.
Spudich, J. L., McCain, D. A., Nakanishi, K., Okabe, M., Shimizu, N., Rodman, H., Honig, B., and Bogomolni, R. A. (1986).Biophys. J. 49, 479–483.
Stern, L. J., Ahl, P. L., Marti, T., Mogi, T., Duñach, M., Berkovitz, S., Rothschild, K. J., and Khorana, H. G. (1989).Biochemistry 28, 10035–10042.
Subramaniam, S., Marti, T., and Khorana, H. G. (1990).Proc. Natl. Acad. Sci. USA 87, 1013–1017.
Subramaniam, S., Greenhalgh, D. A., Rath, P., Rothschild, K. J., and Khorana, H. G. (1991).Proc. Natl. Acad. Sci. USA 88, 6873–6877.
Tittor, J., Soell, C., Oesterhelt, D., Butt, H.-J., and Bamberg, E. (1989).EMBO J. 8, 3477–3482.
Tittor, J., Bamberg, E., and Oesterhelt, D. (1992).J. Bioenerg. Biomembr. 24, 000–000.
Váró, G., and Lanyi, J. K. (1989).Biophys. J. 56, 1143–1151.
Váró, G., and Lanyi, J. K. (1990a).Biochemistry 29, 3798–3804.
Váró, G., and Lanyi, J. K. (1990b).Biochemistry 29, 6858–6865.
Váró, G., and Lanyi, J. K. (1990c).Biochemistry 29, 2241–2250.
Váró, G., and Lanyi, J. K. (1991a).Biochemistry 30, 5008–5015.
Váró, G., and Lanyi, J. K. (1991b).Biophys. J. 59, 313–322.
Váró, G., and Lanyi, J. K. (1991c).Biochemistry 30, 7165–7171.
Váró, G., and Lanyi, J. K. (1991d).Biochemistry 30, 5016–5022.
Váró, G., Zimányi, L., Chang, M. N. B., Needleman, R., and Lanyi, J. K. (1992)Biophys. J. (in press).
Warshel, A. (1978).Proc. Natl. Acad. Sci. USA 75, 2558–2562.
Xie, A. H., Nagle, J. F., and Lozier, R. H. (1987),Biophys. J. 51, 627–635.
Zimányi, L., Keszthelyi, L., and Lanyi, J. K. (1989).Biochemistry 28, 5165–5172.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lanyi, J.K. Proton transfer and energy coupling in the bacteriorhodopsin photocycle. J Bioenerg Biomembr 24, 169–179 (1992). https://doi.org/10.1007/BF00762675
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00762675