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

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.Isotope effects provide deep insight into mechanisms of chemical and biochemical processes. Now, it has been shown that the pattern of isotopic substitution of the isomerizing bond of the retinal chromophore in the visual pigment rhodopsin significantly alters the reaction quantum yield—revealing a vibrational phase-dependent isotope effect.

[1]  M J Tauber,et al.  Wavelength dependent cis-trans isomerization in vision. , 2001, Biochemistry.

[2]  A. Bottoni,et al.  Product formation in rhodopsin by fast hydrogen motions. , 2011, Physical chemistry chemical physics : PCCP.

[3]  Richard A. Mathies,et al.  Vibrational Assignment of Torsional Normal Modes of Rhodopsin: Probing Excited-State Isomerization Dynamics along the Reactive C11C12 Torsion Coordinate , 1998 .

[4]  P. Kukura,et al.  Principles and Applications of Broadband Impulsive Vibrational Spectroscopy. , 2015, The journal of physical chemistry. A.

[5]  M. Garavelli,et al.  Modelling vibrational coherence in the primary rhodopsin photoproduct. , 2012, The Journal of chemical physics.

[6]  Philipp Kukura,et al.  Mode-specificity of vibrationally coherent internal conversion in rhodopsin during the primary visual event. , 2015, Journal of the American Chemical Society.

[7]  R. D. Miller,et al.  Impact of Vibrational Coherence on the Quantum Yield at a Conical Intersection. , 2016, The journal of physical chemistry letters.

[8]  G. Granucci,et al.  Critical appraisal of the fewest switches algorithm for surface hopping. , 2007, The Journal of chemical physics.

[9]  W. Heisenberg,et al.  Zur Quantentheorie der Molekeln , 1924 .

[10]  R. Mathies.  Photochemistry: A coherent picture of vision. , 2015, Nature chemistry.

[11]  D. Zigmantas,et al.  In situ mapping of the energy flow through the entire photosynthetic apparatus. , 2016, Nature chemistry.

[12]  Massimo Olivucci,et al.  Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores. , 2017, Chemical reviews.

[13]  Thom Vreven,et al.  Photoisomerization Path for a Realistic Retinal Chromophore Model: The Nonatetraeniminium Cation , 1998 .

[14]  L. Butler.  Chemical reaction dynamics beyond the Born-Oppenheimer approximation. , 1998, Annual review of physical chemistry.

[15]  Roland Lindh,et al.  The ultrafast photoisomerizations of rhodopsin and bathorhodopsin are modulated by bond length alternation and HOOP driven electronic effects. , 2011, Journal of the American Chemical Society.

[16]  Yoon Sup Lee,et al.  Control of intramolecular orbital alignment in the photodissociation of thiophenol: conformational manipulation by chemical substitution. , 2008, Angewandte Chemie.

[17]  M. Olivucci,et al.  Modulation of thermal noise and spectral sensitivity in Lake Baikal cottoid fish rhodopsins , 2016, Scientific Reports.

[18]  M. Olivucci,et al.  Photoisomerization acceleration in retinal protonated Schiff-base models. , 2003, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[19]  T. Mančal,et al.  Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems , 2007, Nature.

[20]  Jong Min Lim,et al.  Barrierless Photoisomerization of 11-cis Retinal Protonated Schiff Base in Solution. , 2015, Journal of the American Chemical Society.

[21]  Michael Towrie,et al.  On the mechanism of vibrational control of light-induced charge transfer in donor-bridge-acceptor assemblies. , 2015, Nature chemistry.

[22]  Massimo Olivucci,et al.  Relationship between the excited state relaxation paths of rhodopsin and isorhodopsin. , 2008, Journal of the American Chemical Society.

[23]  Felipe Zapata,et al.  Molcas 8: New capabilities for multiconfigurational quantum chemical calculations across the periodic table , 2016, J. Comput. Chem..

[24]  Philipp Kukura,et al.  Sub-10-fs pulses tunable from 480 to 980 nm from a NOPA pumped by an Yb:KGW source. , 2014, Optics letters.

[25]  P. Kollman,et al.  A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules , 1995 .

[26]  Marco Garavelli,et al.  The C 5 H 6 NH 2 + Protonated Shiff Base: An ab Initio Minimal Model for Retinal Photoisomerization , 1997 .

[27]  J. Ponder,et al.  An efficient newton‐like method for molecular mechanics energy minimization of large molecules , 1987 .

[28]  Judith P Klinman,et al.  Hydrogen tunneling links protein dynamics to enzyme catalysis. , 2013, Annual review of biochemistry.

[29]  P. Kukura,et al.  Backbone modification of retinal induces protein-like excited state dynamics in solution. , 2012, Journal of the American Chemical Society.

[30]  R. Miller,et al.  Tracking an electronic wave packet in the vicinity of a conical intersection. , 2017, The Journal of chemical physics.

[31]  R. Mathies,et al.  Conical intersection dynamics of the primary photoisomerization event in vision , 2010, Nature.

[32]  R. Lindh,et al.  Mapping the Excited State Potential Energy Surface of a Retinal Chromophore Model with Multireference and Equation-of-Motion Coupled-Cluster Methods. , 2013, Journal of chemical theory and computation.

[33]  N. Ferré,et al.  Tracking the excited-state time evolution of the visual pigment with multiconfigurational quantum chemistry , 2007, Proceedings of the National Academy of Sciences.

[34]  J. Tully.  Molecular dynamics with electronic transitions , 1990 .

[35]  Vladimir I. Novoderezhkin,et al.  Quantum Coherence in Photosynthesis for Efficient Solar Energy Conversion , 2014, Nature Physics.

[36]  Sang Kyu Kim,et al.  Experimental probing of conical intersection dynamics in the photodissociation of thioanisole. , 2010, Nature chemistry.

[37]  J. Lugtenburg,et al.  Structure of the chromophoric group in bathorhodopsin , 1976, Nature.

[38]  W. Gärtner,et al.  Rhodopsins carrying modified chromophores — the ‘making of’, structural modelling and their light-induced reactivity , 2016, Photochemical and Photobiological Sciences.

[39]  R. Mathies,et al.  Assignment and interpretation of hydrogen out-of-plane vibrations in the resonance Raman spectra of rhodopsin and bathorhodopsin. , 1982, Biochemistry.

[40]  R A Mathies,et al.  The first step in vision: femtosecond isomerization of rhodopsin. , 1991, Science.

[41]  P. Rentzepis,et al.  Primary photochemical event in vision: proton translocation. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[42]  S A Kovalenko,et al.  Femtosecond pump/supercontinuum-probe spectroscopy: optimized setup and signal analysis for single-shot spectral referencing. , 2010, The Review of scientific instruments.

[43]  R. Mathies,et al.  Structural Observation of the Primary Isomerization in Vision with Femtosecond-Stimulated Raman , 2005, Science.

[44]  V. Prokhorenko,et al.  Local vibrational coherences drive the primary photochemistry of vision. , 2015, Nature chemistry.

[45]  G. M. Greetham,et al.  Complete Proton Transfer Cycle in GFP and Its T203V and S205V Mutants** , 2015, Angewandte Chemie.

[46]  G. Kochendoerfer,et al.  Retinal analog study of the role of steric interactions in the excited state isomerization dynamics of rhodopsin. , 1996, Biochemistry.

[47]  S. Kovalenko,et al.  Femtosecond spectroscopy of condensed phases with chirped supercontinuum probing , 1999 .

[48]  R A Mathies,et al.  Vibrationally coherent photochemistry in the femtosecond primary event of vision. , 1994, Science.

[49]  Hohjai Lee,et al.  Coherence Dynamics in Photosynthesis: Protein Protection of Excitonic Coherence , 2007, Science.

[50]  C. Zener.  Non-Adiabatic Crossing of Energy Levels , 1932 .

[51]  Marcus Elstner,et al.  The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. , 2004, Journal of molecular biology.

[52]  R. Mathies,et al.  Chapter 2 The primary photoreaction of rhodopsin , 2000 .

[53]  Massimo Olivucci,et al.  Probing the Photodynamics of Rhodopsins with Reduced Retinal Chromophores. , 2016, Journal of chemical theory and computation.

[54]  Graham R. Fleming,et al.  Two-dimensional spectroscopy of electronic couplings in photosynthesis , 2005, Nature.