Exciton-vibrational resonance and dynamics of charge separation in the photosystem II reaction center

Abstract

The dynamics of charge separation in the photosystem II reaction center (PSII-RC) in the presence of intramolecular vibrations with their frequency matching the energy gap between the exciton state acting as the primary electron donor and the first charge-transfer (CT) state are investigated. A reduced PSII-RC 4-state model explicitly including a CT state is analyzed within Redfield relaxation theory in the multidimensional exciton-vibrational (vibronic) basis. This model is used to study coherent energy/electron transfers and their spectral signatures obtained by two-dimensional electronic spectroscopy (2DES). Modeling of the time-resolved 2D frequency maps obtained by wavelet analysis reveals the origins of the coherences which produce the observed oscillating features in 2DES and allows comparing the lifetimes of the coherences. The results suggest faster excitonic decoherence as compared with longer-lived vibronic oscillations. The emerging picture of the dynamics unravels the role of resonant vibrations in sustaining the effective energy conversion in the PSII-RC. We demonstrate that the mixing of the exciton and CT states promoted by a resonant vibrational quantum allows faster penetration of excitation energy into the CT with subsequent dynamic localization at the bottom of the CT potential induced by the remaining non-resonant nuclear modes. The degree of vibration-assisted mixing and, correspondingly, the rate of primary charge separation, increases significantly in the case of electron-vibrational resonance. The observed features illustrate the principles of quantum design of the photosynthetic unit. These principles are connected with the phenomenon of coherent mixing within vibronic eigenstates, increasing the effectiveness of charge separation not only upon coherent and impulsive laser excitation utilized in the 2DES experiment, but also under natural conditions under non-coherent non-impulsive solar light illumination.

Quantum – coherent dynamics in photosynthetic charge separation revealed by wavelet analysis

“…1). This vibronic mechanism has been proposed and described by theoretical methods [14][15][16][17][18][19][20][21] and later demonstrated by combined experimental-theoretical approaches [11][12][13][22][23][24] . In our previous work 12 , two-dimensional electronic spectroscopy (2DES) [25][26] and Fourier transform (FT) analysis allowed to visualize the coherence between electronic states in 2D frequency maps [obtained by Fourier transformation of the real rephasing 2D spectra along the population time (T)].…”

“…These maps display features corresponding only to the states oscillating at a certain frequency and, therefore, are more selective than the 2D spectra. Moreover, two main 2D frequency maps characteristics: i) the oscillation frequency (in or out of resonance with the electronic states energy gaps), and ii) the position of the most intense bands (corresponding or not to the states in resonance with the oscillation frequency); provide an invaluable tool to classify the observed coherences as mainly electronic, mixed electronic-vibrational (vibronic) or mainly vibrational 11,13,[27][28] . We found that three main frequency modes, 120, 340 and 730 cm -1 , representative of mainly electronic, mixed electronic-vibrational (vibronic) and mainly vibrational coherence, respectively, dominate the oscillatory dynamics 11,13 .…”

“…Moreover, two main 2D frequency maps characteristics: i) the oscillation frequency (in or out of resonance with the electronic states energy gaps), and ii) the position of the most intense bands (corresponding or not to the states in resonance with the oscillation frequency); provide an invaluable tool to classify the observed coherences as mainly electronic, mixed electronic-vibrational (vibronic) or mainly vibrational 11,13,[27][28] . We found that three main frequency modes, 120, 340 and 730 cm -1 , representative of mainly electronic, mixed electronic-vibrational (vibronic) and mainly vibrational coherence, respectively, dominate the oscillatory dynamics 11,13 . The first two types of coherences have functional significance and will be analyzed and discussed below, the non-functional vibrational coherence will be analyzed and discussed in the (P D2 + P D1 − ) δ * ≈690nm , strongly suggesting that charge separation in the PSII RC proceeds via a coherent mechanism 12 .…”

Intramolecular Vibrations Complement the Robustness of Primary Charge Separation in a Dimer Model of the Photosystem II Reaction Center

“…In this work, we focused only on the charge separation starting from the accessory Chl * D1 . As was discussed by Romero et al 15,52 and Fuller et al, 16 however, the charge separation from the special pair (P D1 P D2 ) * cannot be easily discounted. Detailed analyses on the special pair are left for future studies.…”

Calculation of coherences in Förster and modified Redfield theories of excitation energy transfer

“…(a particular case of Eq. (20)). The results of the calculations of the electronic coherence σ 21 (t) within Förster theory according to the derived formula (45) with and without the non-equilibrium correction (54) in comparison with HEOM is presented on Fig.…”