Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Oct;75(4):1689–1699. doi: 10.1016/S0006-3495(98)77611-8

Three electronic state model of the primary phototransformation of bacteriorhodopsin.

W Humphrey 1, H Lu 1, I Logunov 1, H J Werner 1, K Schulten 1
PMCID: PMC1299841  PMID: 9746511

Abstract

The primary all-trans --> 13-cis photoisomerization of retinal in bacteriorhodopsin has been investigated by means of quantum chemical and combined classical/quantum mechanical simulations employing the density matrix evolution method. Ab initio calculations on an analog of a protonated Schiff base of retinal in vacuo reveal two excited states S1 and S2, the potential surfaces of which intersect along the reaction coordinate through an avoided crossing, and then exhibit a second, weakly avoided, crossing or a conical intersection with the ground state surface. The dynamics governed by the three potential surfaces, scaled to match the in situ level spacings and represented through analytical functions, are described by a combined classical/quantum mechanical simulation. For a choice of nonadiabatic coupling constants close to the quantum chemistry calculation results, the simulations reproduce the observed photoisomerization quantum yield and predict the time needed to pass the avoided crossing region between S1 and S2 states at tau1 = 330 fs and the S1 --> ground state crossing at tau2 = 460 fs after light absorption. The first crossing follows after a 30 degrees torsion on a flat S1 surface, and the second crossing follows after a rapid torsion by a further 60 degrees. tau1 matches the observed fluorescence lifetime of S1. Adjusting the three energy levels to the spectral shift of D85N and D212N mutants of bacteriorhodospin changes the crossing region of S1 and S2 and leads to an increase in tau1 by factors 17 and 10, respectively, in qualitative agreement with the observed increase in fluorescent lifetimes.

Full Text

The Full Text of this article is available as a PDF (253.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Braiman M. S., Mogi T., Marti T., Stern L. J., Khorana H. G., Rothschild K. J. Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation changes of aspartic acid residues 85, 96, and 212. Biochemistry. 1988 Nov 15;27(23):8516–8520. doi: 10.1021/bi00423a002. [DOI] [PubMed] [Google Scholar]
  2. Gai F., Hasson K. C., McDonald J. C., Anfinrud P. A. Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin. Science. 1998 Mar 20;279(5358):1886–1891. doi: 10.1126/science.279.5358.1886. [DOI] [PubMed] [Google Scholar]
  3. Govindjee R., Balashov S. P., Ebrey T. G. Quantum efficiency of the photochemical cycle of bacteriorhodopsin. Biophys J. 1990 Sep;58(3):597–608. doi: 10.1016/S0006-3495(90)82403-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Grigorieff N., Ceska T. A., Downing K. H., Baldwin J. M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol. 1996 Jun 14;259(3):393–421. doi: 10.1006/jmbi.1996.0328. [DOI] [PubMed] [Google Scholar]
  5. Hasson K. C., Gai F., Anfinrud P. A. The photoisomerization of retinal in bacteriorhodospin: experimental evidence for a three-state model. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15124–15129. doi: 10.1073/pnas.93.26.15124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990 Jun 20;213(4):899–929. doi: 10.1016/S0022-2836(05)80271-2. [DOI] [PubMed] [Google Scholar]
  7. Humphrey W., Bamberg E., Schulten K. Photoproducts of bacteriorhodopsin mutants: a molecular dynamics study. Biophys J. 1997 Mar;72(3):1347–1356. doi: 10.1016/S0006-3495(97)78781-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996 Feb;14(1):33-8, 27-8. doi: 10.1016/0263-7855(96)00018-5. [DOI] [PubMed] [Google Scholar]
  9. Humphrey W., Logunov I., Schulten K., Sheves M. Molecular dynamics study of bacteriorhodopsin and artificial pigments. Biochemistry. 1994 Mar 29;33(12):3668–3678. doi: 10.1021/bi00178a025. [DOI] [PubMed] [Google Scholar]
  10. Kayanuma Y. Phase coherence and nonadiabatic transition at a level crossing in a periodically driven two-level system. Phys Rev B Condens Matter. 1993 Apr 15;47(15):9940–9943. doi: 10.1103/physrevb.47.9940. [DOI] [PubMed] [Google Scholar]
  11. Kimura Y., Vassylyev D. G., Miyazawa A., Kidera A., Matsushima M., Mitsuoka K., Murata K., Hirai T., Fujiyoshi Y. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature. 1997 Sep 11;389(6647):206–211. doi: 10.1038/38323. [DOI] [PubMed] [Google Scholar]
  12. Lanyi J. K. Mechanism of ion transport across membranes. Bacteriorhodopsin as a prototype for proton pumps. J Biol Chem. 1997 Dec 12;272(50):31209–31212. doi: 10.1074/jbc.272.50.31209. [DOI] [PubMed] [Google Scholar]
  13. Logunov S. L., el-Sayed M. A., Lanyi J. K. Replacement effects of neutral amino acid residues of different molecular volumes in the retinal binding cavity of bacteriorhodopsin on the dynamics of its primary process. Biophys J. 1996 Jun;70(6):2875–2881. doi: 10.1016/S0006-3495(96)79857-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lozier R. H., Bogomolni R. A., Stoeckenius W. Bacteriorhodopsin: a light-driven proton pump in Halobacterium Halobium. Biophys J. 1975 Sep;15(9):955–962. doi: 10.1016/S0006-3495(75)85875-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mathies R. A., Brito Cruz C. H., Pollard W. T., Shank C. V. Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin. Science. 1988 May 6;240(4853):777–779. doi: 10.1126/science.3363359. [DOI] [PubMed] [Google Scholar]
  16. Mogi T., Stern L. J., Marti T., Chao B. H., Khorana H. G. Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4148–4152. doi: 10.1073/pnas.85.12.4148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Needleman R., Chang M., Ni B., Váró G., Fornés J., White S. H., Lanyi J. K. Properties of Asp212----Asn bacteriorhodopsin suggest that Asp212 and Asp85 both participate in a counterion and proton acceptor complex near the Schiff base. J Biol Chem. 1991 Jun 25;266(18):11478–11484. [PubMed] [Google Scholar]
  18. Oesterhelt D., Tittor J., Bamberg E. A unifying concept for ion translocation by retinal proteins. J Bioenerg Biomembr. 1992 Apr;24(2):181–191. doi: 10.1007/BF00762676. [DOI] [PubMed] [Google Scholar]
  19. Otto H., Marti T., Holz M., Mogi T., Stern L. J., Engel F., Khorana H. G., Heyn M. P. Substitution of amino acids Asp-85, Asp-212, and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1018–1022. doi: 10.1073/pnas.87.3.1018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pebay-Peyroula E., Rummel G., Rosenbusch J. P., Landau E. M. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 1997 Sep 12;277(5332):1676–1681. doi: 10.1126/science.277.5332.1676. [DOI] [PubMed] [Google Scholar]
  21. Song L., El-Sayed M. A., Lanyi J. K. Protein catalysis of the retinal subpicosecond photoisomerization in the primary process of bacteriorhodopsin photosynthesis. Science. 1993 Aug 13;261(5123):891–894. doi: 10.1126/science.261.5123.891. [DOI] [PubMed] [Google Scholar]
  22. Subramaniam S., Marti T., Khorana H. G. Protonation state of Asp (Glu)-85 regulates the purple-to-blue transition in bacteriorhodopsin mutants Arg-82----Ala and Asp-85----Glu: the blue form is inactive in proton translocation. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1013–1017. doi: 10.1073/pnas.87.3.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Xu D., Martin C., Schulten K. Molecular dynamics study of early picosecond events in the bacteriorhodopsin photocycle: dielectric response, vibrational cooling and the J, K intermediates. Biophys J. 1996 Jan;70(1):453–460. doi: 10.1016/S0006-3495(96)79588-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Xu D., Sheves M., Schulten K. Molecular dynamics study of the M412 intermediate of bacteriorhodopsin. Biophys J. 1995 Dec;69(6):2745–2760. doi: 10.1016/S0006-3495(95)80146-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Zhou F., Windemuth A., Schulten K. Molecular dynamics study of the proton pump cycle of bacteriorhodopsin. Biochemistry. 1993 Mar 9;32(9):2291–2306. doi: 10.1021/bi00060a022. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES