Elsevier

Chemical Physics

Volume 338, Issues 2–3, 25 September 2007, Pages 168-174
Chemical Physics

Vibrational coherences of the protonated Schiff base of all-trans retinal in solution

https://doi.org/10.1016/j.chemphys.2007.05.019Get rights and content

Abstract

Modulations in the time gated ultrafast fluorescence of the protonated Schiff base of retinal in various solvents are reported, which reflect the creation and evolution of vibrational wave packets due to the torsional mode of retinal of frequency ∼120 cm−1. The oscillations are damped in ∼400 fs. Their frequency is significantly decreased compared to the case of the protein (170 cm−1), and is insensitive to solvent properties such as the dielectric constant and the viscosity. This, along with previous results on mutants of bacteriorhodopsin, leads us to conclude that in the protein, the isomerization dynamics of retinal is governed by steric effects and by the inhomogeneous distribution of the electrostatic field due to amino-acid residues within the protein pocket. We also discuss the origin of the modulations and conclude that they are impulsively excited via the high frequency modes of retinal.

Introduction

For the past 10 years or so, several studies have been carried out on protonated Schiff bases of all-trans retinal (PSBR) in the native protein bacteriorhodopsin (bR), its mutants and in solvents, which aim at identifying the detailed initial events of the photoinduced reaction and their mechanisms. A central issue in these studies is the understanding of how the surrounding environment controls and affects the chromophore early response to photoexcitation. It is known that in bR, the isomerization has a high yield (≈65%) and is selective around the C13double bondC14 double bond [1], while in solvents, the yield is low (<27%) and isomerization occurs around the C9double bondC11, C13double bondC14, C11–C12 bonds [2], [3]. Such large changes between the two environments have either been attributed to electrostatic effects [4], [5], [6], [7], to steric effects [8], [9], [10], or a combination of both, although the two are difficult to disentangle from each other. A further complication comes from the fact that the ultrafast intramolecular dynamics and the intermolecular ones occur concurrently [5], [7], [11], [12].

In order to distinguish between electrostatic and steric effects and between intra- and intermolecular relaxation pathways, it is necessary to tune the environment properties that are expected to contribute to the ultrafast dynamics. Recently, Ruhman and co-workers studied the ultrafast dynamics of PSBR in the native protein and in ethanol using ultrafast transient absorption and stimulated emission spectroscopy [13], [14]. They observed vibrational coherences, whose oscillation frequency changed from 120 cm−1 in solution to 170 cm−1 in the protein. More recently, the same group [15] also reported similar vibrational coherences (in addition to other higher frequency modes) in the protein using impulsive vibrational spectroscopy with 7 fs pulses, which Kobayashi et al. [11] had also reported. The modes corresponding to these coherences have recently been addressed theoretically [16], and experimentally using the normal mode analysis of the Raman spectra [17], [18], and attributed to delocalized skeletal torsional motions of the polyene backbone. From these and other publications [11], [13], [19], [20], it is also now well established that the initial photoinduced event in bR is not the isomerization of retinal, which takes place in 400–500 fs [21]. An ultrafast translocation of charge seems to take place in the first 200 fs or so [19], which is concomitant with the decay of the high frequency modes [11], [22]. Skeletal torsions, eventually excited by IVR from high frequency modes [22], may “guide” the twisting of the chromophore and possibly also control the isomerization rate, as was discussed by Mataga et al. [23], [24] in the case of the photoactive yellow protein (PYP) and its mutants. Excitation of the low frequency modes such as various torsions (not necessarily the torsion around the isomerizing double bond) may deform the chromophore towards the conical intersection with the ground state surface [25], [26], [27], [28].

In order to investigate in more detail the environment effects on the dynamics of PSBR, we recently carried out a comparative study of the ultrafast fluorescence in an extended range of solvents, both protic (methanol MeOH, ethanol EtOH, 2-propanol ProOH, 1-octanol OctOH) and aprotic (acetonitrile ACN, dichloromethane DCM, cyclohexane cHex) differing by over an order of magnitude in dielectric constant or viscosity [10], [29], [30]. Since PSBRs have such largely different isomerization channels and efficiencies in the protein and in solvents, it would appear that the excited-state relaxation times should be good markers of the relaxation pathways and of the way these are influenced by the environment. Overall, we found the relaxation times of the different channels showed no clear dependence on the solvent properties, and in particular, their dielectric constants and protic/aprotic character. Considering the fact that isomerisation leads to a mild structural change of retinal (volume-conserving isomerization), and that the solvent cages are large, we concluded that the protein pocket achieves photocatalytic effect mainly by imposing steric constraints to the PSBR chromophore.

The work of Hou et al. [13], [14] showed that the vibrational coherences provide another marker of the environment, since they found largely different values of the vibrational period in ethanol and in the protein. Here, we report on weak modulations that show up in our ultrafast fluorescence decay curves of PSBR in solvents, and are due to vibrational coherences. Building on our foregoing work, we have investigated their dependence for the same set of solvents used previously [10], [29], [30]. Just as for the decay times, no clear solvent dependence can be identified. This, along with our previous work on the ultrafast fluorescence decay kinetics of PSBR in solvents [10], and on the ultrafast transient absorption of mutants of bR [6], leads us to conclude that in the protein, both steric effects and a specific distribution of the electrostatic field in the protein pocket govern the isomerisation dynamics.

Section snippets

Experimental procedure

Retinal Schiff base cations were prepared according to previously described methods [31] and the sample was protonated either with trichloracetic or trifluoroacetic acid. The nature of the counterion did not affect the spectrotemporal behavior of the PSBR fluorescence. A 250 mL solution of PSBR with OD 10–12 (per cm) is circulated through a 0.5 mm path length flow cell with a speed of 5–6 m/s.

The details of the experimental set-up and methodology have already been given in Refs. [10], [29], [32].

Results

Upon 400 nm excitation the time resolved spectra of all-trans PSBR fluorescence in MeOH span a large spectral range between 440 nm and 900 nm (Fig. 1). It was observed that in the first 100–200 fs the emission narrows down [10], [29], [30], mostly due to the intramolecular relaxation processes, followed by a further narrowing on a slower ps time scale, due to cooling of the chromophore, and finally after 5 ps the emission reaches the vibrationally relaxed shape in all solvents. Before going further,

Discussion and conclusions

Two main questions arise from the above results: (a) What is the origin of the oscillations? (b) Why are they insensitive to the solvent properties?

Vibrational coherences with the same period as reported here were observed by Hou et al. [14] in their transient absorption study of all-trans PSBR in EtOH. Interestingly, the same oscillation was also observed by them in their stimulated emission study of the locked PSBR5.12 chromophore [13], where torsion around the C13–C14 bond is hindered. The

Acknowledgement

This work was supported by the Swiss NSF via contract 2153-065135.03, the NCCR: Quantum Photonics and the PROFIL-2 grant for S.H.

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    Now at Nonlinear Optics and Ultrafast Spectroscopy Laboratory, Sincrotrone Trieste, I-34012 Basovizza Trieste, Italy.

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    Now at Institut de Physique et Chimie des Matériaux de Strasbourg (IPCMS), GONLO, 23, Rue du Loess, F-67034 Strasbourg Cédex, France.

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