Microsolvation of the Redox-Active Tyrosine-D in Photosystem II: Correlation of Energetics with EPR Spectroscopy and Oxidation-Induced Proton Transfer

Abstract

Photosystem II (PSII) of oxygenic photosynthesis captures sunlight to drive the catalytic oxidation of water and the reduction of plastoquinone. Among the several redox-active cofactors that participate in intricate electron transfer pathways there are two tyrosine residues, Y Z and Y D . They are situated in symmetry-related electron transfer branches but have different environments and play distinct roles. Y Z is the immediate oxidant of the oxygen-evolving Mn 4 CaO 5 cluster, whereas Y D serves regulatory and protective functions. The protonation states and hydrogen-bond network in the environment of Y D remain debated, while the role of microsolvation in stabilizing different redox states of Y D and facilitating oxidation or mediating deprotonation, as well the fate of the phenolic proton, is unclear. Here we present detailed structural models of Y D and its environment using large-scale quantum mechanical models and all-atom molecular dynamics of a complete PSII monomer. The energetics of water distribution within a hydrophobic cavity adjacent to Y D are shown to correlate directly with electron paramagnetic resonance (EPR) parameters such as the tyrosyl g -tensor, allowing us to map the correspondence between specific structural models and available experimental observations. EPR spectra obtained under different conditions are explained with respect to the mode of interaction of the proximal water with the tyrosyl radical and the position of the phenolic proton within the cavity. Our results revise previous models of the energetics and build a detailed view of the role of confined water in the oxidation and deprotonation of Y D . Finally, the model of microsolvation developed in the present work rationalizes in a straightforward way the biphasic oxidation kinetics of Y D , offering new structural insights regarding the function of the radical in biological photosynthesis.

Successes, challenges, and opportunities for quantum chemistry in understanding metalloenzymes for solar fuels research

“…182 Similar correlations derived from quantum chemical studies have been essential for probing the hydration and uncovering the structural basis of spectroscopic observations for the other redox-active tyrosine of PSII, Y D . 183 Intriguingly, the above observations suggest a direct role for Ca in structuring the hydrogen-bonding environment of Y Z and hence directly modulating its redox properties, 182 which is crucial for ensuring efficient coupling between the manganese cluster of the OEC and the charge-separation site (reaction centre) of PSII. Complementing this hypothesis, explicit calculations of the effect of calcium substitution by various redox-inactive cations showed that the redox potential of the OEC responds only to the total charge of the cation while remaining insensitive to its Lewis acidity, 190 in contrast to correlations established for synthetic complexes.…”

“…Quantum chemical studies that focus on spectroscopic properties have also helped to elucidate critical aspects of the redox-active tyrosine Y Z and Y D residues. 182,183 Here it is the g-tensor of the tyrosyl radical that is the central spectroscopic parameter. This can be calculated with standard DFT approaches, although particular care has to be taken to ensure that the calculations correctly represent the electronic structure of both the Y Z radical and the Mn cluster.…”

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

“…This is supported by recent computational studies that predict a remarkably short H-bond between Y Z and D1-His190, which is in agreement with the X-ray crystal structure of PSII ( Saito et al., 2011 ; Umena et al., 2011 ). Additionally, quantum mechanical (all-QM) and hybrid quantum mechanical/molecular modeling (QM/MM) studies have suggested that the protonation state of the conjugate base, microsolvation, and hydrogen bonding could influence the redox activity of Y D and Y Z ( Ahlbrink et al., 1998 ; Chai et al., 2019 ; Saito et al., 2011 ; Sirohiwal et al., 2019 ). Since the Y Z ⋅ radical intermediate is short lived, previous mechanistic proposals for PCET were based on the dark-stable Y D ⋅ radical that displays slower decay kinetics.…”

Detection of Water Molecules on the Radical Transfer Pathway of Ribonucleotide Reductase by 17O Electron–Nuclear Double Resonance Spectroscopy

“… 1 Of particular interest is water involvement in electron transfer processes, 2 − 5 its action as a proton wire 6 − 8 or its role in proton-coupled electron transfer (PCET). 9 − 12 The identification of internal water in proteins can be achieved by X-ray diffraction. 13 − 15 However, the crystallization of transient protein complexes is difficult.…”

“…The lack of evidence for a second, almost equivalent water H-bonded to Y 356 • strongly suggests that the two-water model has become very unlikely and alternative explanations for the shifted g x value of Y 356 • will have to be examined. The precise location of second-sphere residues might play a role, 12 which will require further experimental and computational investigation.…”