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Conical intersection dynamics of the primary photoisomerization event in vision

Abstract

Ever since the conversion of the 11-cis retinal chromophore to its all-trans form in rhodopsin was identified as the primary photochemical event in vision1, experimentalists and theoreticians have tried to unravel the molecular details of this process. The high quantum yield of 0.65 (ref. 2), the production of the primary ground-state rhodopsin photoproduct within a mere 200 fs (refs 3–7), and the storage of considerable energy in the first stable bathorhodopsin intermediate8 all suggest an unusually fast and efficient photoactivated one-way reaction9. Rhodopsin's unique reactivity is generally attributed to a conical intersection between the potential energy surfaces of the ground and excited electronic states10,11 enabling the efficient and ultrafast conversion of photon energy into chemical energy12,13,14,15,16. But obtaining direct experimental evidence for the involvement of a conical intersection is challenging: the energy gap between the electronic states of the reacting molecule changes significantly over an ultrashort timescale, which calls for observational methods that combine high temporal resolution with a broad spectral observation window. Here we show that ultrafast optical spectroscopy with sub-20-fs time resolution and spectral coverage from the visible to the near-infrared allows us to follow the dynamics leading to the conical intersection in rhodopsin isomerization. We track coherent wave-packet motion from the photoexcited Franck–Condon region to the photoproduct by monitoring the loss of reactant emission and the subsequent appearance of photoproduct absorption, and find excellent agreement between the experimental observations and molecular dynamics calculations that involve a true electronic state crossing. Taken together, these findings constitute the most compelling evidence to date for the existence and importance of conical intersections in visual photochemistry.

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Figure 1: Wave-packet dynamics through the rhodopsin conical intersection.
Figure 2: Isomerization potential energy surfaces of rhodopsin.
Figure 3: Rhodopsin isomerization probed in the visible spectral range.

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Acknowledgements

M.G., O.W., G.O., G.T. and P.A. thank E4-Computer Engineering S.p.A. for computational time and technical assistance. Part of this study was financially supported by the DFG (FOR490) and by the PRIN programme (2008JKBBK4). P.K. is supported by a Career Acceleration Fellowship awarded by the UK Engineering and Physical Sciences Research Council (EP/H003541/1).

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Contributions

R.A.M., P.K., M.G. and G.C. conceived the project and contributed the original scientific ideas to this work. D.P., C.M. and D.B. executed the experiments. K.M.S. carried out rhodopsin sample preparation/purification. P.A., O.W. and G.O. planned calculations, P.A. and O.W. executed them. G.T. collected calibration data. All authors discussed the results and contributed to the preparation of the manuscript.

Corresponding authors

Correspondence to Marco Garavelli or Giulio Cerullo.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-9 with legends, Supplementary Tables 1-3, a Supplementary Discussion and additional references. (PDF 1757 kb)

Supplementary Movie 1

This movie shows the 11-cis->all-trans photoinduced motion and the frustrated isomerization path - see Supplementary Information file for full legend. (MOV 5994 kb)

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Polli, D., Altoè, P., Weingart, O. et al. Conical intersection dynamics of the primary photoisomerization event in vision. Nature 467, 440–443 (2010). https://doi.org/10.1038/nature09346

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