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

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journal contribution
posted on 2019-03-19, 00:00 authored by Maria Chrysina, Juliana Cecília de Mendonça Silva, Georgia Zahariou, Dimitrios A. Pantazis, Nikolaos Ioannidis
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.