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Arrested Substrate Binding Resolves Catalytic Intermediates in Higher‐Plant Water Oxidation
Author(s) -
Zahariou Georgia,
Ioannidis Nikolaos,
Sanakis Yiannis,
Pantazis Dimitrios A.
Publication year - 2021
Publication title -
angewandte chemie international edition
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 5.831
H-Index - 550
eISSN - 1521-3773
pISSN - 1433-7851
DOI - 10.1002/anie.202012304
Subject(s) - chemistry , electron paramagnetic resonance , photosystem ii , oxygen evolving complex , catalysis , substrate (aquarium) , crystallography , catalytic cycle , photochemistry , metastability , oxidizing agent , site directed spin labeling , spin states , reaction intermediate , photosynthesis , inorganic chemistry , membrane , organic chemistry , nuclear magnetic resonance , biochemistry , physics , oceanography , geology
Among the intermediate catalytic steps of the water‐oxidizing Mn 4 CaO 5 cluster of photosystem II (PSII), the final metastable S 3 state is critically important because it binds one substrate and precedes O 2 evolution. Herein, we combine X‐ and Q‐band EPR experiments on native and methanol‐treated PSII of Spinacia oleracea and show that methanol‐treated PSII preparations of the S 3 state correspond to a previously uncharacterized high‐spin ( S= 6) species. This is confirmed as a major component also in intact photosynthetic membranes, coexisting with the previously known intermediate‐spin conformation ( S= 3). The high‐spin intermediate is assigned to a water‐unbound form, with a Mn IV 3 subunit interacting ferromagnetically via anisotropic exchange with a coordinatively unsaturated Mn IV ion. These results resolve and define the structural heterogeneity of the S 3 state, providing constraints on the S 3 to S 4 transition, on substrate identity and delivery pathways, and on the mechanism of O−O bond formation.