A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation

Abstract

Photosystem II (PS II) captures solar energy and directs charge separation (CS) across the thylakoid membrane during photosynthesis. The highly oxidizing, charge-separated state generated within its reaction center (RC) drives water oxidation. Spectroscopic studies on PS II RCs are difficult to interpret due to large spectral congestion, necessitating modeling to elucidate key spectral features. Herein, we present results from time-dependent density functional theory (TDDFT) calculations on the largest PS II RC model reported to date. This model explicitly includes six RC chromophores and both the chlorin phytol chains and the amino acid residues <6 Å from the pigments’ porphyrin ring centers. Comparing our wild-type model results with calculations on mutant D1-His-198-Ala and D2-His-197-Ala RCs, our simulated absorption-difference spectra reproduce experimentally observed shifts in known chlorophyll absorption bands, demonstrating the predictive capabilities of this model. We find that inclusion of both nearby residues and phytol chains is necessary to reproduce this behavior. Our calculations provide a unique opportunity to observe the molecular orbitals that contribute to the excited states that are precursors to CS. Strikingly, we observe two high oscillator strength, low-lying states, in which molecular orbitals are delocalized over ChlD1 and PheD1 as well as one weaker oscillator strength state with molecular orbitals delocalized over the P chlorophylls. Both these configurations are a match for previously identified exciton–charge transfer states (ChlD1+PheD1−)* and (PD2+PD1−)*. Our results demonstrate the power of TDDFT as a tool, for studies of natural photosynthesis, or indeed future studies of artificial photosynthetic complexes.

How Can We Predict Accurate Electrochromic Shifts for Biochromophores? A Case Study on the Photosynthetic Reaction Center

“…Analogous results have been reported before when calculations are performed in the absence of the protein. 25 , 86 , 115 , 116 Importantly, even when the geometric strain imposed by the protein is included implicitly by using QM/MM-optimized geometries for these gas-phase excited state calculations, as in the present work, no excitonic asymmetry in terms of strongly differentiated site energies arises in the RC. 25 This starkly highlights the necessity of adequately capturing the effect of protein electrostatics, because this is the only way of achieving a meaningful computational representation of the physical system.…”

Protein Matrix Control of Reaction Center Excitation in Photosystem II

“…Therefore, the use of experimental geometries introduces a fundamental inconsistency between the quantum chemical approach and the structural model on which it operates, leading to randomization of results through uncontrolled errors. When this is coupled with the neglect of protein matrix electrostatics, the combined methodological deficiencies practically guarantee that the quantum chemical results are of little relevance to the real system (for example, a study that satisfies none of these conditions finds the lowest-energy excitation of the RC to be localized on the Pheo D1 ). The same holds for the direct use of force-field (MM) geometries .…”

The origin of unidirectional charge separation in photosynthetic reaction centers: nonadiabatic quantum dynamics of exciton and charge in pigment–protein complexes

“…34 The quantitative values of excitation energies may depend on functionals and parameters. 32,38,67 The 6-31G(d) basis set is used for all the QM calculations.…”