Proton Transfer and Energy Coupling in the Bacteriorhodopsin Photocycle

Overview

Journal J Bioenerg Biomembr

Publisher Springer

Specialties Biochemistry
Biology
Endocrinology

Date 1992 Apr 1

PMID 1326515

Citations 32

Authors

J K Lanyi

Affiliations

Soon will be listed here.

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 in equilibrium with L in equilibrium with M1----M2 in equilibrium with N in equilibrium with O----BR, where coupling to the proton-motive force is at the energetically and mechanistically important M1----M2 step. The consequences of site-specific mutations expressed homologously in Halobacterium 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.

Citing Articles

Actinorhodopsin: an efficient and robust light-driven proton pump for bionanotechnological applications.

Ayoub N, Djabeur N, Harder D, Jeckelmann J, Ucurum Z, Hirschi S Sci Rep. 2025; 15(1):4054.

PMID: 39900604 PMC: 11790970. DOI: 10.1038/s41598-025-88055-8.

Reversible Photochromic Reactions of Bacteriorhodopsin from at Femto- and Picosecond Times.

Smitienko O, Feldman T, Shelaev I, Gostev F, Aybush A, Cherepanov D Molecules. 2024; 29(20).

PMID: 39459214 PMC: 11510181. DOI: 10.3390/molecules29204847.

Diversity, Mechanism, and Optogenetic Application of Light-Driven Ion Pump Rhodopsins.

Inoue K Adv Exp Med Biol. 2021; 1293:89-126.

PMID: 33398809 DOI: 10.1007/978-981-15-8763-4_6.

Unifying photocycle model for light adaptation and temporal evolution of cation conductance in channelrhodopsin-2.

Kuhne J, Vierock J, Tennigkeit S, Dreier M, Wietek J, Petersen D Proc Natl Acad Sci U S A. 2019; 116(19):9380-9389.

PMID: 31004059 PMC: 6510988. DOI: 10.1073/pnas.1818707116.

The evolving capabilities of rhodopsin-based genetically encoded voltage indicators.

Gong Y Curr Opin Chem Biol. 2015; 27:84-9.

PMID: 26143170 PMC: 4571180. DOI: 10.1016/j.cbpa.2015.05.006.

References

Kakitani H, Kakitani T, Rodman H, Honig B . On the mechanism of wavelength regulation in visual pigments. Photochem Photobiol. 1985; 41(4):471-9. DOI: 10.1111/j.1751-1097.1985.tb03514.x. View

Henderson R, Baldwin J, Ceska T, Zemlin F, Beckmann E, Downing K . Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990; 213(4):899-929. DOI: 10.1016/S0022-2836(05)80271-2. View

Milder S . Correlation between absorption maxima and thermal isomerization rates in bacteriorhodopsin. Biophys J. 2009; 60(2):440-6. PMC: 1260081. DOI: 10.1016/S0006-3495(91)82070-7. View

Mogi T, Stern L, Marti T, Chao B, Khorana H . Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc Natl Acad Sci U S A. 1988; 85(12):4148-52. PMC: 280383. DOI: 10.1073/pnas.85.12.4148. View

Oesterhelt D, Tittor J, Bamberg E . A unifying concept for ion translocation by retinal proteins. J Bioenerg Biomembr. 1992; 24(2):181-91. DOI: 10.1007/BF00762676. View

Zimanyi L, Keszthelyi L, Lanyi J . Transient spectroscopy of bacterial rhodopsins with an optical multichannel analyzer. 1. Comparison of the photocycles of bacteriorhodopsin and halorhodopsin. Biochemistry. 1989; 28(12):5165-72. DOI: 10.1021/bi00438a038. View

Lozier R, Bogomolni R, Stoeckenius W . Bacteriorhodopsin: a light-driven proton pump in Halobacterium Halobium. Biophys J. 1975; 15(9):955-62. PMC: 1334761. DOI: 10.1016/S0006-3495(75)85875-9. View

Tittor J, Soell C, Oesterhelt D, Butt H, Bamberg E . A defective proton pump, point-mutated bacteriorhodopsin Asp96----Asn is fully reactivated by azide. EMBO J. 1989; 8(11):3477-82. PMC: 401504. DOI: 10.1002/j.1460-2075.1989.tb08512.x. View

de Groot H, Smith S, Courtin J, van den Berg E, Winkel C, Lugtenburg J . Solid-state 13C and 15N NMR study of the low pH forms of bacteriorhodopsin. Biochemistry. 1990; 29(29):6873-83. DOI: 10.1021/bi00481a017. View

10.

Dancshazy Z, Govindjee R, Ebrey T . Independent photocycles of the spectrally distinct forms of bacteriorhodopsin. Proc Natl Acad Sci U S A. 1988; 85(17):6358-61. PMC: 281970. DOI: 10.1073/pnas.85.17.6358. View

11.

Varo G, Lanyi J . Pathways of the rise and decay of the M photointermediate(s) of bacteriorhodopsin. Biochemistry. 1990; 29(9):2241-50. DOI: 10.1021/bi00461a006. View

12.

Mathies R, Lin S, Ames J, Pollard W . 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. View

13.

de Groot H, Harbison G, Herzfeld J, Griffin R . Nuclear magnetic resonance study of the Schiff base in bacteriorhodopsin: counterion effects on the 15N shift anisotropy. Biochemistry. 1989; 28(8):3346-53. DOI: 10.1021/bi00434a033. View

14.

Braiman M, Mathies R . Resonance Raman spectra of bacteriorhodopsin's primary photoproduct: evidence for a distorted 13-cis retinal chromophore. Proc Natl Acad Sci U S A. 1982; 79(2):403-7. PMC: 345751. DOI: 10.1073/pnas.79.2.403. View

15.

Mowery P, Lozier R, Chae Q, Tseng Y, Taylor M, Stoeckenius W . Effect of acid pH on the absorption spectra and photoreactions of bacteriorhodopsin. Biochemistry. 1979; 18(19):4100-7. DOI: 10.1021/bi00586a007. View

16.

Ames J, Mathies R . The role of back-reactions and proton uptake during the N----O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study. Biochemistry. 1990; 29(31):7181-90. DOI: 10.1021/bi00483a005. View

17.

Nagle J, Parodi L, Lozier R . Procedure for testing kinetic models of the photocycle of bacteriorhodopsin. Biophys J. 1982; 38(2):161-74. PMC: 1328891. DOI: 10.1016/S0006-3495(82)84543-8. View

18.

Otto H, Marti T, Holz M, Mogi T, Stern L, Engel F . 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; 87(3):1018-22. PMC: 53401. DOI: 10.1073/pnas.87.3.1018. View

19.

Ort D, Parson W . The quantum yield of flash-induced proton release by bacteriorhodopsin-containing membrane fragments. Biophys J. 1979; 25(2 Pt 1):341-53. PMC: 1328469. DOI: 10.1016/s0006-3495(79)85296-0. View

20.

Balashov S, Govindjee R, Ebrey T . Redshift of the purple membrane absorption band and the deprotonation of tyrosine residues at high pH: Origin of the parallel photocycles of trans-bacteriorhodopsin. Biophys J. 2009; 60(2):475-90. PMC: 1260085. DOI: 10.1016/S0006-3495(91)82074-4. View