Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2000 Apr;78(4):2031–2036. doi: 10.1016/S0006-3495(00)76750-6

The effect of protein conformation change from alpha(II) to alpha(I) on the bacteriorhodopsin photocycle.

J Wang 1, M A El-Sayed 1
PMCID: PMC1300795  PMID: 10733981

Abstract

The bacteriorhodopsin (bR) photocycle was followed by use of time-resolved Fourier-transform infrared (FTIR) spectroscopy as a function of temperature (15-85 degrees C) as the alpha(II) --> alpha(I) conformational transition occurs. The photocycle rate increases with increasing temperature, but its efficiency is found to be drastically reduced as the transition takes place. A large shift is observed in the all-trans left arrow over right arrow 13-cis equilibrium due to the increased stability of the 13-cis isomer in alpha(I) form. This, together with the increase in the rate of dark adaptation as the temperature increases, leads to a large increase in the 13-cis isomer concentration in bR in the alpha(I) form. The fact that 13-cis retinal has a much-reduced absorption cross-section and its inability to pump protons leads to an observed large reduction in the concentration of the observed photocycle intermediates, as well as the proton gradient at a given light intensity. These results suggest that nature might have selected the alpha(II) rather than the alpha(I) form as the helical conformation in bR to stabilize the all-trans retinal isomer that is a better light absorber and is capable of pumping protons.

Full Text

The Full Text of this article is available as a PDF (78.1 KB).

Selected References

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

  1. Birge R. R. Photophysics of light transduction in rhodopsin and bacteriorhodopsin. Annu Rev Biophys Bioeng. 1981;10:315–354. doi: 10.1146/annurev.bb.10.060181.001531. [DOI] [PubMed] [Google Scholar]
  2. Braiman M. S., Bousché O., Rothschild K. J. Protein dynamics in the bacteriorhodopsin photocycle: submillisecond Fourier transform infrared spectra of the L, M, and N photointermediates. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2388–2392. doi: 10.1073/pnas.88.6.2388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dencher N. A., Dresselhaus D., Zaccai G., Büldt G. Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7876–7879. doi: 10.1073/pnas.86.20.7876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Hessling B., Souvignier G., Gerwert K. A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. Biophys J. 1993 Nov;65(5):1929–1941. doi: 10.1016/S0006-3495(93)81264-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Jackson M. B., Sturtevant J. M. Phase transitions of the purple membranes of Halobacterium halobium. Biochemistry. 1978 Mar 7;17(5):911–915. doi: 10.1021/bi00598a026. [DOI] [PubMed] [Google Scholar]
  7. Koch M. H., Dencher N. A., Oesterhelt D., Plöhn H. J., Rapp G., Büldt G. Time-resolved X-ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin. EMBO J. 1991 Mar;10(3):521–526. doi: 10.1002/j.1460-2075.1991.tb07978.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Krimm S., Dwivedi A. M. Infrared spectrum of the purple membrane: clue to a proton conduction mechanism? Science. 1982 Apr 23;216(4544):407–408. doi: 10.1126/science.6280277. [DOI] [PubMed] [Google Scholar]
  9. Mathies R. A., Lin S. W., Ames J. B., Pollard W. T. From femtoseconds to biology: mechanism of bacteriorhodopsin's light-driven proton pump. Annu Rev Biophys Biophys Chem. 1991;20:491–518. doi: 10.1146/annurev.bb.20.060191.002423. [DOI] [PubMed] [Google Scholar]
  10. Nakasako M., Kataoka M., Amemiya Y., Tokunaga F. Crystallographic characterization by X-ray diffraction of the M-intermediate from the photo-cycle of bacteriorhodopsin at room temperature. FEBS Lett. 1991 Nov 4;292(1-2):73–75. doi: 10.1016/0014-5793(91)80837-s. [DOI] [PubMed] [Google Scholar]
  11. Ormos P., Chu K., Mourant J. Infrared study of the L, M, and N intermediates of bacteriorhodopsin using the photoreaction of M. Biochemistry. 1992 Aug 4;31(30):6933–6937. doi: 10.1021/bi00145a010. [DOI] [PubMed] [Google Scholar]
  12. Pfefferlé J. M., Maeda A., Sasaki J., Yoshizawa T. Fourier transform infrared study of the N intermediate of bacteriorhodopsin. Biochemistry. 1991 Jul 2;30(26):6548–6556. doi: 10.1021/bi00240a027. [DOI] [PubMed] [Google Scholar]
  13. Schulte A., Bradley L., 2nd High-pressure near-infrared Raman spectroscopy of bacteriorhodopsin light to dark adaptation. Biophys J. 1995 Oct;69(4):1554–1562. doi: 10.1016/S0006-3495(95)80027-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Stockburger M., Klusmann W., Gattermann H., Massig G., Peters R. Photochemical cycle of bacteriorhodopsin studied by resonance Raman spectroscopy. Biochemistry. 1979 Oct 30;18(22):4886–4900. doi: 10.1021/bi00589a017. [DOI] [PubMed] [Google Scholar]
  15. Stoeckenius W., Lozier R. H. Light energy conversion in Halobacterium halobium. J Supramol Struct. 1974;2(5-6):769–774. doi: 10.1002/jss.400020519. [DOI] [PubMed] [Google Scholar]
  16. Subramaniam S., Gerstein M., Oesterhelt D., Henderson R. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 1993 Jan;12(1):1–8. doi: 10.1002/j.1460-2075.1993.tb05625.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Taneva S. G., Caaveiro J. M., Muga A., Goñi F. M. A pathway for the thermal destabilization of bacteriorhodopsin. FEBS Lett. 1995 Jul 3;367(3):297–300. doi: 10.1016/0014-5793(95)00570-y. [DOI] [PubMed] [Google Scholar]
  18. Torres J., Sepulcre F., Padrós E. Conformational changes in bacteriorhodopsin associated with protein-protein interactions: a functional alpha I-alpha II helix switch? Biochemistry. 1995 Dec 19;34(50):16320–16326. doi: 10.1021/bi00050a012. [DOI] [PubMed] [Google Scholar]
  19. Tsuda M., Ebrey T. G. Effect of high pressure on the absorption spectrum and isomeric composition of bacteriorhodopsin. Biophys J. 1980 Apr;30(1):149–157. doi: 10.1016/S0006-3495(80)85083-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tuzi S., Naito A., Saitô H. 13C NMR study on conformation and dynamics of the transmembrane alpha-helices, loops, and C-terminus of [3-13C]Ala-labeled bacteriorhodopsin. Biochemistry. 1994 Dec 20;33(50):15046–15052. doi: 10.1021/bi00254a013. [DOI] [PubMed] [Google Scholar]
  21. Vogel H., Gärtner W. The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy. J Biol Chem. 1987 Aug 25;262(24):11464–11469. [PubMed] [Google Scholar]
  22. Wang J., El-Sayed M. A. Temperature jump-induced secondary structural change of the membrane protein bacteriorhodopsin in the premelting temperature region: a nanosecond time-resolved Fourier transform infrared study. Biophys J. 1999 May;76(5):2777–2783. doi: 10.1016/S0006-3495(99)77431-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES