Three Electronic State Model of the Primary Phototransformation of Bacteriorhodopsin

Abstract

The primary all-trans --> 13-cis photoisomerization of retinal in bacteriorhodopsin has been investigated by means of quantum chemical and combined classical/quantum mechanical simulations employing the density matrix evolution method. Ab initio calculations on an analog of a protonated Schiff base of retinal in vacuo reveal two excited states S1 and S2, the potential surfaces of which intersect along the reaction coordinate through an avoided crossing, and then exhibit a second, weakly avoided, crossing or a conical intersection with the ground state surface. The dynamics governed by the three potential surfaces, scaled to match the in situ level spacings and represented through analytical functions, are described by a combined classical/quantum mechanical simulation. For a choice of nonadiabatic coupling constants close to the quantum chemistry calculation results, the simulations reproduce the observed photoisomerization quantum yield and predict the time needed to pass the avoided crossing region between S1 and S2 states at tau1 = 330 fs and the S1 --> ground state crossing at tau2 = 460 fs after light absorption. The first crossing follows after a 30 degrees torsion on a flat S1 surface, and the second crossing follows after a rapid torsion by a further 60 degrees. tau1 matches the observed fluorescence lifetime of S1. Adjusting the three energy levels to the spectral shift of D85N and D212N mutants of bacteriorhodospin changes the crossing region of S1 and S2 and leads to an increase in tau1 by factors 17 and 10, respectively, in qualitative agreement with the observed increase in fluorescent lifetimes.

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

“…23 for earlier dynamics) unambiguously demonstrated the flat character of the excited state surface and the presence of a small barrier. Therefore, the ''three-state'' model (24,27,28), proposed that both the S 1 (B u ) and S 2 (A g ) states are involved in the dynamics of the excited state photoisomerization. In this model, a flat part of the potential surface along the torsional coordinate and the barrier were numerically evaluated as a result of the S 1 and S 2 states coupling and their avoided crossing.…”

Development of Ultrafast Spectroscopy and Reaction Mechanisms Studied by the Observation of Ultrashort-Life Species and Transition States

“…This pump is optically triggered by transcis photoisomerization, which is closely related to cistrans photoisomerization of rhodopsin in the vision process 48 even though the reaction is in the opposite direction. Because of these interesting physiological and artificial functionalities, the primary process of bR has been extensively studied both theoretically 49,50 and experimentally. 5157 Most studies made up to now 42 consider the primary photoprocess to be described as follows:…”

“…60 The J intermediate is often assigned as a ground-state species in which the retinal chromophore is isomerized to a 13-cis-configuration, as first proposed by the group of Ruhman. 58 Furthermore, two theoretical models of photoisomerization have been proposed, namely a two-state, two-mode model and a three-state model proposed by groups of Olivucci 49,61 and Schulten; 50,62 it still remains unclear which model is correct. Recent studies of photoisomerization of retinyl chromophore have shed light on the dynamics after photoexcitation; 63,64 however, the details of the transient states still remain contentious.…”

Molecular dynamics of strained retinal in various electronic states

“…In Refs. [13,14] quasicrossings of S 0 , S 1 , and S 2 states were investigated. Unfortunately, nonadiabatic rotary dynamics of retinal can be described only at a model level.…”

“…For example, in Ref. [14] nondiagonal elements of Hamiltonian are replaced with material parameters not dependent on the torsion angle. Although isentropic potentials of the three states are determined with sufficiently high accuracy [CASSCF (8,8) 6-31G], the computational algorithm does not provide optimization of the geometric configuration in the case of variations in the torsion angle.…”