Dynamic protein conformations preferentially drive energy transfer along the active chain of the photosystem II reaction centre

Abstract

One longstanding puzzle concerning photosystem II, a core component of photosynthesis, is that only one of the two symmetric branches in its reaction centre is active in electron transfer. To investigate the effect of the photosystem II environment on the preferential selection of the energy transfer pathway (a prerequisite for electron transfer), we have constructed an exciton model via extensive molecular dynamics simulations and quantum mechanics/molecular mechanics calculations based on a recent X-ray structure. Our results suggest that it is essential to take into account an ensemble of protein conformations to accurately compute the site energies. We identify the cofactor CLA606 of active chain as the most probable site for the energy excitation. We further pinpoint a number of charged protein residues that collectively lower the CLA606 site energy. Our work provides insights into the understanding of molecular mechanisms of the core machinery of the green-plant photosynthesis.

Quantum Chemical Studies of Light Harvesting

“…493 Recently, the crystal structure of the PSII complex of Thermosynechococcus vulcanus has been refined at 1.9 Å resolution, allowing determination of the positions of the atoms involved in the Mn4CaO5 cluster of the oxygen-evolving complex. 433 The new structure, in addition, suggests some structural differences among the active and inactive chains, and has been used in more recent structure-based studies by Zhang et al in order to explore the impact of protein dynamics, explored using MD simulations, on semiempirical QM/MM estimates of the site energies, 494 and by Frankcombe to compute the excited-states in the complex from a multi-monomer supermolecule calculation performed at the TD-DFT level using the long-range corrected CAM-B3LYP functional. 495 Interestingly, the study by Zhang et al suggests that protein dynamics preferentially drive the energy transfer along the active chain of PSII.…”

Molecular dynamics simulations in photosynthesis

“…In most studies, two-dimensional electronic spectra were calculated by using experimental observables to obtain several modeling parameters as e.g., done for LH2 (van der Vegte et al 2015) and Fenna-Matthews-Olson (FMO) complex (Olbrich et al 2011a). Also, the dynamics in the excited states were simulated e.g., for LH2 (van der Vegte et al 2015), LH3 (Mallus et al 2018), and the bacterial reaction center (Vassiliev and Bruce 2006;Zhang et al 2014;Hsieh et al 2019) based on snapshots extracted from MD simulations. From a theoretical point of view, including the protein environment in calculations of electronic states is challenging.…”

“…Example studies of its impact on the electronically excited states were performed for the FMO complex (Olbrich et al 2011b;Vassiliev et al 2011) and the bacterial reaction center (Narzi et al , 2017. The impact of nanosecond protein fluctuations on excitation energy transfer and charge separation were evaluated as well for bacterial reaction centers (Vassiliev and Bruce 2006;Zhang et al 2014;Hsieh et al 2019;Kulik et al 2020). MD simulations coupled to quantum chemical calculations permitted also to gain insights in the couplings of selected pairs of chlorophylls (López-Tarifa et al 2017) and excitation energy quenching via carotenoids in LHCII Maity et al 2019).…”

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

“…The full exciton model of the PSII-RC includes the excited states of 8 pigments (6 chlorophylls (Chl) and 2 pheophytins (Phe)) coupled to several (at least 4) charge-transfer (CT) states. 3,5,9,[23][24][25][26][27][28] The explicit modeling of exciton-vibrational dynamics for such a 12-state model (that requires a 12-dimensional configuration space) is too complicated numerically, but the essential spectral properties and excited-state dynamics can be explored by reducing the model to a smaller number of states. For example, the absorption and 2DFT spectra of the PSII-RC can be described by a reduced 4-state model 7 that includes two central chlorophylls (special pair) P D1 and P D2 and the pigments from the active branch, i.e.…”