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⇱ Local vibrational coherences drive the primary photochemistry of vision | Nature Chemistry

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Abstract

The role of vibrational coherence—concerted vibrational motion on the excited-state potential energy surface—in the isomerization of retinal in the protein rhodopsin remains elusive, despite considerable experimental and theoretical efforts. We revisited this problem with resonant ultrafast heterodyne-detected transient-grating spectroscopy. The enhanced sensitivity that this technique provides allows us to probe directly the primary photochemical reaction of vision with sufficient temporal and spectral resolution to resolve all the relevant nuclear dynamics of the retinal chromophore during isomerization. We observed coherent photoproduct formation on a sub-50 fs timescale, and recovered a host of vibrational modes of the retinal chromophore that modulate the transient-grating signal during the isomerization reaction. Through Fourier filtering and subsequent time-domain analysis of the transient vibrational dynamics, the excited-state nuclear motions that drive the isomerization reaction were identified, and comprise stretching, torsional and out-of-plane wagging motions about the local C11=C12 isomerization coordinate.

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Figure 1: The linear absorption spectrum of rhodopsin.
Figure 2: Transient-grating spectroscopy of rhodopsin.
Figure 3: Vibrational dynamics of retinal isomerization in rhodopsin.
Figure 4: Localized excited-state vibrational modes of the retinal chromophore in rhodopsin.

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Acknowledgements

P.J.M.J. thanks J.M. Morrow and B.S.W. Chang for many helpful discussions and shared laboratory equipment during the early stages of this work. L. Chen is acknowledged for excellent technical assistance. This research was supported by the Natural Sciences and Engineering Research Council of Canada (R.J.D.M.), the Max Planck Society (R.J.D.M.), the Canadian Institute for Advanced Research (R.J.D.M. and O.P.E.) and the Canada Excellence Research Chair program (O.P.E.). O.P.E. is the Anne & Max Tanenbaum Chair in Neuroscience at the University of Toronto.

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Authors and Affiliations

  1. Institute for Optical Sciences and Departments of Chemistry and Physics, University of Toronto, 80 St George Street, Toronto, M5S 3H6, Ontario, Canada

    Philip J. M. Johnson, Alexei Halpin & R. J. Dwayne Miller

  2. Department of Biochemistry, University of Toronto, 1 King's College Circle, Toronto, M5S 1A8, Ontario, Canada

    Takefumi Morizumi & Oliver P. Ernst

  3. Atomically Resolved Dynamics Division, Max Planck Institute for the Structure and Dynamics of Matter, Building 99 (CFEL), Luruper Chaussee 149, Hamburg, 22761, Germany

    Valentyn I. Prokhorenko & R. J. Dwayne Miller

  4. Department of Molecular Genetics, University of Toronto, 1 King's College Circle, Toronto, M5S 1A8, Ontario, Canada

    Oliver P. Ernst

Authors
  1. Philip J. M. Johnson
  2. Alexei Halpin
  3. Takefumi Morizumi
  4. Valentyn I. Prokhorenko
  5. Oliver P. Ernst
  6. R. J. Dwayne Miller

Contributions

P.J.M.J., A.H. and V.I.P. constructed the instruments. T.M. prepared and characterized the sample. P.J.M.J. and A.H. performed the measurements. P.J.M.J and V.I.P. analysed the data. P.J.M.J. wrote the manuscript with editing from all authors. O.P.E. and R.J.D.M. supervised the project.

Corresponding author

Correspondence to R. J. Dwayne Miller.

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The authors declare no competing financial interests.

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Johnson, P., Halpin, A., Morizumi, T. et al. Local vibrational coherences drive the primary photochemistry of vision. Nature Chem 7, 980–986 (2015). https://doi.org/10.1038/nchem.2398

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