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Proton Translocation via Tautomerization of Asn298 During the S₂–S₃ State Transition in the Oxygen-Evolving Complex of Photosystem II

Chrysina, Maria, de Mendonça Silva, Juliana Cecília, Zahariou, Georgia, Pantazis, Dimitrios A., Ioannidis, Nikolaos
TheJournal of physical chemistry 2019 v.123 no.14 pp. 3068-3078
deuterium oxide, electron paramagnetic resonance spectroscopy, electron transfer, freezing, hydrogen bonding, isotopes, lighting, models, oxidation, oxygen evolving complex, quinones, tautomerization, temperature, tyrosine
In biological water oxidation, a redox-active tyrosine residue (D1-Tyr161 or YZ) mediates electron transfer between the Mn₄CaO₅ cluster of the oxygen-evolving complex and the charge-separation site of photosystem II (PSII), driving the cluster through progressively higher oxidation states Sᵢ (i = 0–4). In contrast to lower S-states (S₀, S₁), in higher S-states (S₂, S₃) of the Mn₄CaO₅ cluster, YZ cannot be oxidized at cryogenic temperatures due to the accumulation of positive charge in the S₁ → S₂ transition. However, oxidation of YZ by illumination of S₂ at 77–190 K followed by rapid freezing and charge recombination between YZ• and the plastoquinone radical QA•– allows trapping of an S₂ variant, the so-called S₂ᵗʳᵃᵖᵖᵉᵈ state (S₂ᵗ), that is capable of forming YZ• at cryogenic temperature. To identify the differences between the S₂ and S₂ᵗ states, we used the S₂ᵗYZ• intermediate as a probe for the S₂ᵗ state and followed the S₂ᵗYZ•/QA•– recombination kinetics at 10 K using time-resolved electron paramagnetic resonance spectroscopy in H₂O and D₂O. The results show that while S₂ᵗYZ•/QA•– recombination can be described as pure electron transfer occurring in the Marcus inverted region, the S₂ᵗ → S₂ reversion depends on proton rearrangement and exhibits a strong kinetic isotope effect. This suggests that YZ oxidation in the S₂ᵗ state is facilitated by favorable proton redistribution in the vicinity of YZ, most likely within the hydrogen-bonded YZ–His190–Asn298 triad. Computational models show that tautomerization of Asn298 to its imidic acid form enables proton translocation to an adjacent asparagine-rich cavity of water molecules that functions as a proton reservoir and can further participate in proton egress to the lumen.