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Evidence for a vibrational phase-dependent isotope effect on the photochemistry of vision

Abstract

Vibronic coupling is key to efficient energy flow in molecular systems and a critical component of most mechanisms invoking quantum effects in biological processes. Despite increasing evidence for coherent coupling of electronic states being mediated by vibrational motion, it is not clear how and to what degree properties associated with vibrational coherence such as phase and coupling of atomic motion can impact the efficiency of light-induced processes under natural, incoherent illumination. Here, we show that deuteration of the H11–C11=C12–H12 double-bond of the 11-cis retinal chromophore in the visual pigment rhodopsin significantly and unexpectedly alters the photoisomerization yield while inducing smaller changes in the ultrafast isomerization dynamics assignable to known isotope effects. Combination of these results with non-adiabatic molecular dynamics simulations reveals a vibrational phase-dependent isotope effect that we suggest is an intrinsic attribute of vibronically coherent photochemical processes.

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Fig. 1
Fig. 2: Isomerization quantum yields for native, 11,12-H2 regenerated and isotopically labelled retinal chromophores in rhodopsin obtained at an excitation wavelength of 532 nm.
Fig. 3: Transient absorption measurements and corresponding fitting results of rhodopsin regenerated with retinal chromophores with different patterns of isotopic substitution about the isomerizing C11=C12 double bond.
Fig. 4: Simulated excited-state isomerization dynamics of bovine rhodopsin.
Fig. 5: 2D-modelling of simulated rhodopsin population dynamics.

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Acknowledgements

We acknowledge support from the National Eye Institute for providing 11-cis retinal used to make the 11,12-H2 regenerated rhodopsin sample. P.K. was supported by the EPSRC (EP/K006630/1). M.O. is supported by the NSF (CHE-1710191) and HFSP (RGP0049/2012) and also thanks the Ohio Supercomputer Center for computer time. I.S. is supported by the ERC Starting Grant ‘PhotoMutant’ (678169). This work was supported in part by the Mathies Royalty Fund.

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R.A.M. and J.L. conceived the project. P.K., C.S. and M.L. designed all experiments and analysed the data. J.L. and I.F. synthesized the isotopomers. M.O. and X.Y. carried out the molecular dynamics simulations and developed the proposed theoretical model. I.S. and A.V. wrote the isotope simulation code. K.M.S. prepared the rhodopsin samples for all measurements. C.S., P.K., M.O. and R.A.M. wrote the manuscript with contributions from all other authors.

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Correspondence to M. Olivucci or P. Kukura or R. A. Mathies.

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Supplementary Data and Analysis, Supplementary Figures 1–17, Tables 1–3

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Schnedermann, C., Yang, X., Liebel, M. et al. Evidence for a vibrational phase-dependent isotope effect on the photochemistry of vision. Nature Chem 10, 449–455 (2018). https://doi.org/10.1038/s41557-018-0014-y

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