Comparative investigation of the photoisomerization of the protonated and unprotonated n-butylamine Schiff bases of 9-cis-, 11-cis-, 13-cis-, and all-trans-retinals

151

146

Ab initio methods are used to characterize the ground and first excited state of the chromophore in the rhodopsin family of proteins: retinal protonated Schiff base. Retinal protonated Schiff base has five double bonds capable of undergoing isomerization. Upon absorption of light, the chromophore isomerizes and the character of the photoproducts (e.g., 13-cis and 11-cis) depends on the environment, protein vs. solution. Our ab initio calculations show that, in the absence of any specific interactions with the environment (e.g., discrete ordered charges in a protein), energetic considerations cannot explain the observed bond selectivity. We instead attribute the origin of bond selectivity to the shape (topography) of the potential energy surfaces in the vicinity of points of true degeneracy (conical intersections) between the ground and first excited electronic states. This provides a molecular example where a competition between two distinct but nearly isoenergetic photochemical reaction pathways is resolved by a topographical difference between two conical intersections.O ne of the simplest means to convert light into mechanical motion at the atomic scale is cis-trans photoisomerization, and it is widely used in photoactive proteins. Retinal protonated Schiff base (RPSB) is the best known biological chromophore, with five double bonds capable of undergoing photoisomerization. A long-standing question has been the mechanism that selects the isomerizing bond, particularly the role of the protein environment in ''steering'' reactivity. The availability of the structures of rhodopsin (1) and bacteriorhodopsin (2-5), coupled with characterization of RPSB solution-phase photochemistry (6-11), provides a unique opportunity to identify this mechanism. Conical intersections (CIs), geometries where two electronic states are truly degenerate, providing doorways from excited to ground electronic states, are widely believed to be important in photochemistry (12)(13)(14), and their role in photoinduced isomerization has been well documented (14-22). However, their role in bond torsion selectivity has yet to be established. In this paper, we show that the topography, or shape, around CIs determines this selectivity in RPSB. This direct connection between CI topography and photochemical selectivity has significant implications for understanding protein ''steering'' and the rational design of molecular optoelectronic devices.Investigations of the photochemistry of RPSB have established that the protein is not an idle spectator; quantum yield, selectivity, and time scales are all significantly different in solution and protein environments. In the protein environment, isomerization occurs exclusively around a single bond, e.g., 11-cis 3 all-trans in rhodopsin and all-trans 3 13-cis in bacteriorhodopsin. In contrast, illumination of the all-trans chromophore in solution results in several photoproducts with 11-cis being the most dominant (6-8). The isomerization quantum yield is greater than 50% in proteins (23), but rarely excee...

Section: Sketchmentioning

confidence: 72%

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confidence: 97%

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confidence: 99%

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The role of intersection topography in bond selectivity ofcis-transphotoisomerization

Ben‐Nun

Molnár

Schulten

et al. 2002

151

146

“…Retinal in solution shows relatively slow and nonselective photoisomerization around several double bonds (12)(13)(14) with low yield. The specific ultrafast, all-trans, 13-cis photoisomerization of the retinal in bR is the purple membrane photosynthesis key event which has a quantum yield of 55%.…”

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confidence: 99%

The relaxation dynamics of the excited electronic states of retinal in bacteriorhodopsin by two-pump-probe femtosecond studies

Logunov

Volkov

Braun

et al. 2001

We present the results of two-pump and probe femtosecond experiments designed to follow the relaxation dynamics of the lowest excited state (S 1) populated by different modes. In the first mode, a direct (S0 3 S1) radiative excitation of the ground state is used. In the second mode, an indirect excitation is used where the S 1 state is populated by the use of two femtosecond laser pulses with different colors and delay times between them. The first pulse excites the S 0 3 S1 transition whereas the second pulse excites the S 1 3 Sn transition. The nonradiative relaxation from the Sn state populates the lowest excited state. Our results suggest that the S 1 state relaxes faster when populated nonradiatively from the Sn state than when pumped directly by the S0 3 S1 excitation. Additionally, the S n 3 S1 nonradiative relaxation time is found to change by varying the delay time between the two pump pulses. The observed dependence of the lowest excited state population as well as its dependence on the delay between the two pump pulses are found to fit a kinetic model in which the S n state populates a different surface (called S 1) than the one being directly excited (S 1). The possible involvement of the Ag type states, the J intermediate, and the conical intersection leading to the S 0 or to the isomerization product (K intermediate) are discussed in the framework of the proposed model. Halobacterium salinarum (Halobium salinarium) is a member of Halobacteria, which is part of the domain Archaea. In an anaerobic condition under light illumination, H. salinarum demonstrates a pH decrease in cell suspension and ATP synthesis (1, 2), the main features of photosynthesis. The photosynthetic activity in H. salinarum was attributed to bacteriorhodopsin (bR), a 26-kDa protein that is hexagonally packed within the purple membrane (1-4). Since the discovery of the purple membrane, its enigmatically efficient photosynthesis is in the center of the most active research. To our surprise, the archaic organism effectively utilizes more than 50% of the absorbed light energy (5, 6).Retinal, a light-absorbing polyene, is the bR chromophore and is linked to its Lys-216 by a protonated Schiff base. The chromophore undergoes light-induced isomerization and masters proton transfer across the membrane (7-11). The photoisomerization of retinal initiates a series of retinal protein structural reconformations of the bacteriorhodopsin that lead to the formation of different intermediates and finally return it to its initial state with all-trans-retinal. Overall, this photocycle consists of at least seven intermediates of bR with different visible absorption spectra and lifetimes bR 568 3 S 1 3 J 3 K 630 3 L 550 3 M 412 3 N 520 3 O 640 3 bR 568 (4).Retinal in solution shows relatively slow and nonselective photoisomerization around several double bonds (12-14) with low yield. The specific ultrafast, all-trans, 13-cis photoisomerization of the retinal in bR is the purple membrane photosynthesis key event which has a quantum yield of 55%. The p...

“…Enumerating all the cis͞trans isomers yields 2 5 ϭ 32 different possibilities. Photoexcitation of all-trans retinal linked to a protonated Schiff base in methanol solution yields cis isomers with an overall quantum efficiency of Ϸ0.15, with 11-cis accounting for Ϸ75% of the photoproducts (11,34). In bR, photoexcitation of all-trans retinal yields the 13-cis form with quantum efficiency of Ϸ0.…”

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confidence: 99%

The photoisomerization of retinal in bacteriorhodopsin: Experimental evidence for a three-state model

Hasson

Gai

Anfinrud

1996

185

228

The primary events in the all-trans to 13-cis photoisomerization of retinal in bacteriorhodopsin have been investigated with femtosecond time-resolved absorbance spectroscopy. Spectra measured over a broad range extending from 7000 to 22,400 cm ؊1 reveal features whose dynamics are inconsistent with a model proposed earlier to account for the highly efficient photoisomerization process. Emerging from this work is a new three-state model. Photoexcitation of retinal with visible light accesses a shallow well on the excited state potential energy surface. This well is bounded by a small barrier, arising from an avoided crossing that separates the Franck-Condon region from the nearby reactive region of the photoisomerization coordinate. At ambient temperatures, the reactive region is accessed with a time constant of Ϸ500 fs, whereupon the retinal rapidly twists and encounters a second avoided crossing region. The protein mediates the passage into the second avoided crossing region and thereby exerts control over the quantum yield for forming 13-cis retinal. The driving force for photoisomerization resides in the retinal, not in the surrounding protein. This view contrasts with an earlier model where photoexcitation was thought to access directly a reactive region of the excited-state potential and thereby drive the retinal to a twisted conformation within 100-200 fs.