Impact of Electronic State Mixing on the Photoisomerization Time Scale of the Retinal Chromophore

Abstract

Spectral data show that the photoisomerization of retinal protonated Schiff base (rPSB) chromophores occurs on a 100 fs time scale or less in vertebrate rhodopsins, it is several times slower in microbial rhodopsins and it is between one and 2 orders of magnitude slower in solution. These time scale variations have been attributed to specific modifications of the topography of the first excited state potential energy surface of the chromophore. However, it is presently not clear which specific environment effects (e.g., electrostatic, electronic, or steric) are responsible for changing the surface topography. Here, we use QM/MM models and excited state trajectory computations to provide evidence for an increase in electronic mixing between the first and the second excited state of the chromophore when going from vertebrate rhodopsin to the solution environments. Ultimately, we argue that a correlation between the lifetime of the first excited state and electronic mixing between such state and its higher neighbor, may have been exploited to evolve rhodopsins toward faster isomerization and, possibly, light-sensitivity.

Fluorescence Enhancement of a Microbial Rhodopsin via Electronic Reprogramming

“…In other words, we provide support for a structure of the L83Q and W76S/Y179F PESs and related dynamics consistent with the left and right diagram of Scheme 1B respectively. 29…”

“…However, the trapping occurs in WT and W76S/Y179F (for WT see also our previous report. 29 In these cases, the S 2 and S 1 profiles cross (or couple) periodically generating “islands” with increased non-reactive 2Ag character. These islands are characterized by BLA oscillations (see also Figure 5 below) which modulate the S 1 and S 2 gap and the associated 1Bu/2Ag character mixing.…”

Anabaena Sensory Rhodopsin: Effect of point mutations on PSBR photo-isomerization speed

“…The acceleration of the photo-isomerization reaction in blue-shifted mutants suggests a steeper slope of the excited state potential energy surface (PES) than in WT-ASR. This can be tentatively explained by a lifted degeneracy between the S1 and S2 states upon mutations, in contrast to AT WT-ASR where electronic mixing between S1 and S2 is more prominent, thus inducing a flat PES in the vicinity of the Franck-Condon region [5]. A detailed QM/MM simulation is in progress.…”

Fluorescence Enhancement of a Microbial Rhodopsin via Electronic Reprogramming

“…These are labeled 1Ag, 1Bu, and 2Ag (consistent with the electronic terms of a homologous all-trans polyene with C 2h symmetry). 25,27 S 1 has a 1Bu character characterized by a positive charge spread (i.e. transferred) towards the H 2 C=CH− end of the PSB5 framework.…”

“…The electronic states driving the photoisomerization of model retinal chromophores have originally been described by Josef Michl and Vlasta Bonacǐć Koutecky. 27,28 Below we assume that the ESL is determined by the chromophore S 1 reactivity. In other words, the isomerization motion on S 1 , leading to fast nonradiative decay through a CI between the S 1 and S 0 PESs, is held responsible for the sub-picosecond ESL and the low fluorescence quantum yield (QY).…”