Modelling Time-Resolved Two-Dimensional Electronic Spectroscopy of the Primary Photoisomerization Event in Rhodopsin

Time-resolved two-dimensional (2D) electronic spectra (ES) tracking the evolution of the excited state manifolds of the retinal chromophore have been simulated along the photoisomerization pathway in bovine rhodopsin, using a state-of-the-art hybrid QM/MM approach based on multiconfigurational methods. Simulations of broadband 2D spectra provide a useful picture of the overall detectable 2D signals from the near-infrared (NIR) to the near-ultraviolet (UV). Evolution of the stimulated emission (SE) and excited state absorption (ESA) 2D signals indicates that the S1 → SN (with N ≥ 2) ESAs feature a substantial blue-shift only after bond inversion and partial rotation along the cis → trans isomerization angle, while the SE rapidly red-shifts during the photoinduced skeletal relaxation of the polyene chain. Different combinations of pulse frequencies are proposed in order to follow the evolution of specific ESA signals. These include a two-color 2DVis/NIR setup especially suited for tracking the evolution of the S1 → S2 transitions that can be used to discriminate between different photochemical mechanisms of retinal photoisomerization as a function of the environment. The reported results are consistent with the available time-resolved pump–probe experimental data, and may be used for the design of more elaborate transient 2D electronic spectroscopy techniques.

[1]  Peifang Tian,et al.  Femtosecond Phase-Coherent Two-Dimensional Spectroscopy , 2003, Science.

[2]  S. Mukamel,et al.  Multidimensional femtosecond correlation spectroscopies of electronic and vibrational excitations. , 2000, Annual review of physical chemistry.

[3]  Martin T. Zanni,et al.  Concepts and Methods of 2D Infrared Spectroscopy , 2011 .

[4]  Manfred Burghammer,et al.  Structure of bovine rhodopsin in a trigonal crystal form. , 2003, Journal of molecular biology.

[5]  P. Anfinrud,et al.  Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin. , 1998, Science.

[6]  Matthew A. Montgomery,et al.  Facile collection of two-dimensional electronic spectra using femtosecond pulse-shaping Technology. , 2007, Optics express.

[7]  T. Okada,et al.  Crystallographic analysis of primary visual photochemistry. , 2006, Angewandte Chemie.

[8]  Jennifer P. Ogilvie,et al.  Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes , 2004 .

[9]  Marco Garavelli,et al.  A tunable QM/MM approach to chemical reactivity, structure and physico-chemical properties prediction , 2007 .

[10]  G. Fleming,et al.  Tunable two-dimensional femtosecond spectroscopy. , 2004, Optics letters.

[11]  Walter Thiel,et al.  QM/MM methods for biomolecular systems. , 2009, Angewandte Chemie.

[12]  S. Mukamel.  Principles of Nonlinear Optical Spectroscopy , 1995 .

[13]  K. Palczewski,et al.  Crystal Structure of Rhodopsin: A G‐Protein‐Coupled Receptor , 2002, Chembiochem : a European journal of chemical biology.

[14]  Frank Terstegen,et al.  ABSOLUTE SENSE OF TWIST OF THE C12-C13 BOND OF THE RETINAL CHROMOPHORE IN RHODOPSIN : SEMIEMPIRICAL AND NONEMPIRICAL CALCULATIONS OF CHIROPTICAL DATA , 1998 .

[15]  Björn O. Roos,et al.  Second-order perturbation theory with a complete active space self-consistent field reference function , 1992 .

[16]  Martin Schütz,et al.  Molpro: a general‐purpose quantum chemistry program package , 2012 .

[17]  Tomoyuki Hayashi,et al.  Coherent multidimensional vibrational spectroscopy of biomolecules: concepts, simulations, and challenges. , 2009, Angewandte Chemie.

[18]  FRANCESCO AQUILANTE,et al.  MOLCAS 7: The Next Generation , 2010, J. Comput. Chem..

[19]  K. T. Compton.  The American Institute of Physics , 1933 .

[20]  Giulio Cerullo,et al.  Disentangling Peptide Configurations via Two-Dimensional Electronic Spectroscopy: Ab Initio Simulations Beyond the Frenkel Exciton Hamiltonian , 2014, The journal of physical chemistry letters.

[21]  Holger Gohlke,et al.  The Amber biomolecular simulation programs , 2005, J. Comput. Chem..

[22]  R. Hochstrasser,et al.  Two-dimensional infrared spectroscopy: a promising new method for the time resolution of structures. , 2001, Current opinion in structural biology.

[23]  N. Ferré,et al.  Quantum chemical modeling and preparation of a biomimetic photochemical switch. , 2007, Angewandte Chemie.

[24]  K. Palczewski,et al.  Crystal Structure of Rhodopsin: A G‐Protein‐Coupled Receptor , 2000, Science.

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

[26]  Marco Garavelli,et al.  Initial Excited-State Relaxation of the Isolated 11-cis Protonated Schiff Base of Retinal: Evidence for in-Plane Motion from ab Initio Quantum Chemical Simulation of the Resonance Raman Spectrum , 1999 .

[27]  Per-Åke Malmqvist,et al.  Multiconfiguration perturbation theory with imaginary level shift , 1997 .

[28]  Marco Garavelli,et al.  Modelling retinal chromophores photoisomerization: from minimal models in vacuo to ultimate bidimensional spectroscopy in rhodopsins. , 2014, Physical chemistry chemical physics : PCCP.

[29]  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.

[30]  Björn O. Roos,et al.  The CASSCF state interaction method , 1989 .

[31]  Andrew M. Moran,et al.  Two-Dimensional Electronic Spectroscopy in the Ultraviolet Wavelength Range. , 2012, The journal of physical chemistry letters.

[32]  Marco Garavelli,et al.  Electrostatic control of the photoisomerization efficiency and optical properties in visual pigments: on the role of counterion quenching. , 2009, Journal of the American Chemical Society.

[33]  R. Mathies,et al.  The first step in vision occurs in femtoseconds: complete blue and red spectral studies. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D C Teller,et al.  Crystal structure of rhodopsin: a template for cone visual pigments and other G protein-coupled receptors. , 2002, Biochimica et biophysica acta.

[35]  Paolo Villoresi,et al.  Few-optical-cycle pulses tunable from the visible to the mid-infrared by optical parametric amplifiers , 2009 .

[36]  K. Schulten,et al.  Molecular Dynamics Studies of Bacteriorhodopsin's Photocycles , 1995 .

[37]  Krzysztof Palczewski,et al.  Crystal structure of a photoactivated deprotonated intermediate of rhodopsin , 2006, Proceedings of the National Academy of Sciences.

[38]  S. Mukamel,et al.  The coupled electronic oscillators vs the sum‐over‐states pictures for the optical response of octatetraene , 1996 .

[39]  R. Birge.  Photophysics and molecular electronic applications of the rhodopsins. , 1990, Annual review of physical chemistry.

[40]  T. Okada,et al.  Local peptide movement in the photoreaction intermediate of rhodopsin , 2006, Proceedings of the National Academy of Sciences.

[41]  M Olivucci,et al.  Computational evidence in favor of a two-state, two-mode model of the retinal chromophore photoisomerization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  M. Chergui,et al.  Coherent ultrafast torsional motion and isomerization of a biomimetic dipolar photoswitch. , 2010, Physical chemistry chemical physics : PCCP.

[44]  K. P. Lawley,et al.  Ab initio methods in quantum chemistry , 1987 .

[45]  Giulio Cerullo,et al.  Ab Initio Simulations of Two-Dimensional Electronic Spectra: The SOS//QM/MM Approach , 2014 .

[46]  Marco Garavelli,et al.  Probing and modeling the absorption of retinal protein chromophores in vacuo. , 2010, Angewandte Chemie.

[47]  Oliver P. Ernst,et al.  Crystal structure of metarhodopsin II , 2011, Nature.

[48]  D. Baylor,et al.  How photons start vision. , 1996, Proceedings of the National Academy of Sciences of the United States of America.