Theoretical explanation of efficient non-radiative deactivation of zeaxanthin

We present a detailed TD-DFT/DFT analysis of light absorption by the carotenoid pigment zeaxanthin (Zea), which plays an important role in photosynthesis and photoprotection. Zea can exist in six conformations determined by the rotation of the cyclohexene rings (RR, RL, LL, TT, RT, and LT), each of which was modeled separately. To accurately theoretically reproduce the optical properties of this pigment, the M11 functional was selected. Combined with the 6-31++G(d,p) basis set and the IEFPCM solvent model, we obtain a good agreement between the calculated and experimental absorption spectra. Zea's vibronic transitions and the excited-state vibrations they activate were analyzed. These vibrations were found to be very large-scale, utilizing a large fraction of the Zea molecule and thus capable of efficiently transferring the energy gained from photoexcitation to the surrounding medium. For the first time, we obtained the S₂ profile of the excited state of Zea along the ring rotation. Compared to a ground-state one, we found that the R → T, T → R, L → T, and T → L conformational transitions are hindered upon excitation, while R → L and L → R transitions are facilitated. Since the proportions of RR, RL, and LL conformers significantly predominate over the others, light irradiation of Zea actually promotes its conformational transitions. We assume a significant role of vibrational relaxation of the pigment molecule in the S₁ state: vibration of the alternating stretching-compression of single and double bonds of the polyene chain has a huge intensity and can effectively transfer the vibrational energy of Zea to the environment. Photoinduced electron density shifts in the Zea molecule were also obtained. The redistributions of electron density accompanying S₂ → S₁ and S₁ → S₀ relaxations are much more significant than for S₀ → S₂ excitation.