Modelling the role of internal flexibility and inter-state couplings modulated by an explicit environment in the absorption spectrum of coelenteramide

Recently developed mixed quantum classical (MQC) approaches, which integrate classical molecular dynamics (MD) driven by accurate quantum-mechanically derived force fields with vibronic models, were employed to investigate the absorption spectra in benzene solution of coelenteramide, the chromophore of different photoproteins. Our results confirm that light absorption in this medium is only due to the protonated neutral species 2H. Neglecting the large-amplitude motions of the most flexible modes and adopting local harmonic expansions of the potential energy surfaces around the global minimum, the simulation of the spectrum is straightforward and it even leads to decent agreement with the experiment, indicating only moderate nonadiabatic effects. The complexity of the molecule becomes however evident when trying to accurately describe the effect of molecular flexibility, a key property expected to be very sensitive to the protein environment. MD sampling in fact shows that at room temperature the 2H molecule frequently assumes conformations where its excited electronic states are almost degenerate and hence strongly mix, with drastic redistribution of the oscillator strengths. We document that such mixings are triggered by both stiff vibrations and soft flexible modes and that, in such a complex scenario, methods that do not properly describe nonadiabatic interactions at the quantum vibronic level introduce artifacts in the simulation of the spectrum. We also show that such problems can be cured, at least approximately, by resorting to the parameterization of linear vibronic coupling models specific for the different configurations sampled from the classical MD. A critical discussion of all achieved results is eventually addressed, hence setting up a robust grounding for further development of MQC protocols for electronic spectroscopy of flexible dyes in the condensed phase.