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Untangling the sequence of events during the S₂ → S₃ transition in photosystem II and implications for the water oxidation mechanism.

ABSTRACT: In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S₁, S₂, S₃, and S₀, showing that a water molecule is inserted during the S₂ → S₃ transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O₂ formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S₂ → S₃ transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, Q_A and Q_B, are observed. At the donor site, tyrosine Y_Z and His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of O_X(H) at the open coordination site of Mn1. This water, possibly a ligand of Ca, could be supplied via a "water wheel"-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 µs) during the S₂ → S₃ transition mirrors the appearance of O_X electron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.

SUBMITTER: Ibrahim M

PROVIDER: S-EPMC7293653 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Untangling the sequence of events during the S2 → S3 transition in photosystem II and implications for the water oxidation mechanism.

Ibrahim Mohamed M Fransson Thomas T Chatterjee Ruchira R Cheah Mun Hon MH Hussein Rana R Lassalle Louise L Sutherlin Kyle D KD Young Iris D ID Fuller Franklin D FD Gul Sheraz S Kim In-Sik IS Simon Philipp S PS de Lichtenberg Casper C Chernev Petko P Bogacz Isabel I Pham Cindy C CC Orville Allen M AM Saichek Nicholas N Northen Trent T Batyuk Alexander A Carbajo Sergio S Alonso-Mori Roberto R Tono Kensuke K Owada Shigeki S Bhowmick Asmit A Bolotovsky Robert R Mendez Derek D Moriarty Nigel W NW Holton James M JM Dobbek Holger H Brewster Aaron S AS Adams Paul D PD Sauter Nicholas K NK Bergmann Uwe U Zouni Athina A Messinger Johannes J Kern Jan J Yachandra Vittal K VK Yano Junko J

Proceedings of the National Academy of Sciences of the United States of America 20200520 23

In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2 → S3 transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of even ...[more]

PMID: 32434915

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Project description:In this paper, we combine broken symmetry density functional calculations and electron paramagnetic resonance analysis to obtain the electronic structure of the penultimate S3 state of nature's water-oxidizing complex and determine the electronic pathway of O-O bond formation. Analysis of the electronic structure changes along the reaction path shows that two spin crossovers, facilitated by the geometry and magnetism of the water-oxidizing complex, are used to provide a unique low-energy pathway. The pathway is facilitated via the formation and stabilization of the [O2]3- ion. This ion is formed between ligated deprotonated substrate waters, O5 and O6, and is stabilized by antiferromagnetic interaction with the Mn ions of the complex. Combining the computational, crystallographic, and spectroscopic data, we show that an equilibrium exists between the O5 oxo and O6 hydroxo forms with an S = 3 spin state and a deprotonated O6 form containing a two-center one-electron bond in [O5O6]3- which we identify as the form detected using crystallography. This form corresponds to an S = 6 spin state which we demonstrate gives rise to a low-intensity EPR spectrum compared with the accompanying S = 3 state, making its detection via EPR difficult and overshadowed by the S = 3 form. Simulations using 70% of the S = 6 component give rise to a superior fit to the experimental W-band EPR spectral envelope compared with an S = 3 only form. Analyses of the most recent X-ray emission spectroscopy first moment changes for solution and time-resolved crystal data are also shown to support the model. The computational, crystallographic, and spectroscopic data are shown to coalesce to the same picture of a predominant S = 6 species containing the first one-electron oxidation product of two water molecules, that is, [O5O6]3-. Progression of this form to the two-electron-oxidized peroxo and three-electron-oxidized superoxo forms, leading eventually to the evolution of triplet O2, is proposed to be the pathway nature adopts to oxidize water. The study reveals the key electronic, magnetic, and structural design features of nature's catalyst which facilitates water oxidation to O2 under ambient conditions.

Dataset Information

Untangling the sequence of events during the S₂ → S₃ transition in photosystem II and implications for the water oxidation mechanism.

Publications

Untangling the sequence of events during the S<sub>2</sub> → S<sub>3</sub> transition in photosystem II and implications for the water oxidation mechanism.

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