The retinal chromophore/chloride ion pair: Structure of the photoisomerization path and interplay of charge transfer and covalent states

doi:10.1073/pnas.0408723102

The retinal chromophore/chloride ion pair: Structure of the photoisomerization path and interplay of charge transfer and covalent states

^†Dipartimento di Chimica “G. Ciamician,” Università di Bologna, Via Selmi 2, I-40126 Bologna, Italy; ^§Dipartimento di Chimica, Università di Siena, Via Aldo Moro, I-53100 Siena, Italy; and ^¶Centro per lo Studio dei Sistemi Complessi, Via Tommaso Pendola 37, I-53100 Siena, Italy

Edited by Joshua Jortner, Tel Aviv University, Tel Aviv, Israel, and approved March 10, 2005 (received for review November 24, 2004)

Abstract

Ab initio multireference second-order perturbation theory computations are used to explore the photochemical behavior of two ion pairs constituted by a chloride counterion interacting with either a rhodopsin or bacteriorhodopsin chromophore model (i.e., the 4-cis-γ-methylnona-2,4,6,8-tetraeniminium and all-trans-nona-2,4,6,8-tetraeniminium cations, respectively). Significant counterion effects on the structure of the photoisomerization paths are unveiled by comparison with the paths of the same chromophores in vacuo. Indeed, we demonstrate that the counterion (i) modulates the relative stability of the S₀, S₁, and S₂ energy surfaces leading to an S₁ isomerization energy profile where the S₁ and S₂ states are substantially degenerate; (ii) leads to the emergence of significant S₁ energy barriers along all of the isomerization paths except the one mimicking the 11-cis → all-trans isomerization of the rhodopsin chromophore model; and (iii) changes the nature of the S₁ → S₀ decay funnel that becomes a stable excited state minimum when the isomerizing double bond is located at the center of the chromophore moiety. We show that these (apparently very different) counterion effects can be rationalized on the basis of a simple qualitative electrostatic model, which also provides a crude basis for understanding the behavior of retinal protonated Schiff bases in solution.

Footnotes

↵ ∥ To whom correspondence may be sent at the § or ¶ address. E-mail: olivucci{at}unisi.it.
†† To whom correspondence may be addressed. E-mail: marco.garavelli{at}unibo.it.
↵ ‡ Present address: Department of Chemistry and Supercomputing Institute, University of Minnesota, Minneapolis, MN 55455-0431.
Author contributions: F.B. and M.G. designed research; A.C. performed research; M.O. and M.G. analyzed data; and M.O. and M.G. wrote the paper.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations: bR, bacteriorhodopsin; FC, Franck-Condon; CI, conical intersection; CAS-SCF, complete active space-self consistent field; MEP, minimum energy path; PSB, protonated Schiff base; QY, quantum yield; Rh, rhodopsin; SP, stationary point; TICT, twisted intramolecular charge transfer; TM, true energy minima; TS, transition state.
↵ ‡‡ Obviously, the residual β-ionone ring conjugation and its alkyl inductive effects are not accounted for in our models.
↵ §§ Because translocation of the counterion to the central position of the chromophore chain (i.e., above the central double bond of models 1 and 2) is predicted to leave the original energy gap unchanged (due to an equivalent stabilization of the charge transfer and covalent states), a systematic trend may be expected at the TICT points, with decreasing S₁-S₀ energy separation as decreasing the distance between the twisted central double bond and the counterion (see ref. 11).