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Structures of the intermediates of Kok's photosynthetic water oxidation clock.

ABSTRACT: Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model for photosynthetic oxygen evolution, known as Kok's S-state clock or cycle^1,2. The model comprises four (meta)stable intermediates (S₀, S₁, S₂ and S₃) and one transient S₄ state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn₄CaO₅) cluster in the oxygen-evolving complex^3-7. This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone Q_B at the acceptor side of PSII. Here, using serial femtosecond X-ray crystallography and simultaneous X-ray emission spectroscopy with multi-flash visible laser excitation at room temperature, we visualize all (meta)stable states of Kok's cycle as high-resolution structures (2.04-2.08 Å). In addition, we report structures of two transient states at 150 and 400 µs, revealing notable structural changes including the binding of one additional 'water', Ox, during the S₂→S₃ state transition. Our results suggest that one water ligand to calcium (W3) is directly involved in substrate delivery. The binding of the additional oxygen Ox in the S₃ state between Ca and Mn1 supports O-O bond formation mechanisms involving O5 as one substrate, where Ox is either the other substrate oxygen or is perfectly positioned to refill the O5 position during O₂ release. Thus, our results exclude peroxo-bond formation in the S₃ state, and the nucleophilic attack of W3 onto W2 is unlikely.

SUBMITTER: Kern J

PROVIDER: S-EPMC6485242 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Structures of the intermediates of Kok's photosynthetic water oxidation clock.

Kern Jan J Chatterjee Ruchira R Young Iris D ID Fuller Franklin D FD Lassalle Louise L Ibrahim Mohamed M Gul Sheraz S Fransson Thomas T Brewster Aaron S AS Alonso-Mori Roberto R Hussein Rana R Zhang Miao M Douthit Lacey L de Lichtenberg Casper C Cheah Mun Hon MH Shevela Dmitry D Wersig Julia J Seuffert Ina I Sokaras Dimosthenis D Pastor Ernest E Weninger Clemens C Kroll Thomas T Sierra Raymond G RG Aller Pierre P Butryn Agata A Orville Allen M AM Liang Mengning M Batyuk Alexander A Koglin Jason E JE Carbajo Sergio S Boutet Sébastien S Moriarty Nigel W NW Holton James M JM Dobbek Holger H Adams Paul D PD Bergmann Uwe U Sauter Nicholas K NK Zouni Athina A Messinger Johannes J Yano Junko J Yachandra Vittal K VK

Nature 20181107 7731

Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model for photosynthetic oxygen evolution, known as Kok's S-state clock or cycle1,2. The model comprises four (meta)stable intermediates (S0, S1, S2 and S3) and one transient S4 state, which precedes dioxygen formation occurring in a concert ...[more]

PMID: 30405241

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Project description:A barrier to understanding the factors driving catalysis in the oxygen evolution reaction (OER) is understanding multiple overlapping redox transitions in the OER catalysts. The complexity of these transitions obscure the relationship between the coverage of adsorbates and OER kinetics, leading to an experimental challenge in measuring activity descriptors, such as binding energies, as well as adsorbate interactions, which may destabilize intermediates and modulate their binding energies. Herein, we utilize a newly designed optical spectroelectrochemistry system to measure these phenomena in order to contrast the behavior of two electrocatalysts, cobalt oxyhydroxide (CoOOH) and cobalt-iron hexacyanoferrate (cobalt-iron Prussian blue, CoFe-PB). Three distinct optical spectra are observed in each catalyst, corresponding to three separate redox transitions, the last of which we show to be active for the OER using time-resolved spectroscopy and electrochemical mass spectroscopy. By combining predictions from density functional theory with parameters obtained from electroadsorption isotherms, we demonstrate that a destabilization of catalytic intermediates occurs with increasing coverage. In CoOOH, a strong (∼0.34 eV/monolayer) destabilization of a strongly bound catalytic intermediate is observed, leading to a potential offset between the accumulation of the intermediate and measurable O2 evolution. We contrast these data to CoFe-PB, where catalytic intermediate generation and O2 evolution onset coincide due to weaker binding and destabilization (∼0.19 eV/monolayer). By considering a correlation between activation energy and binding strength, we suggest that such adsorbate driven destabilization may account for a significant fraction of the observed OER catalytic activity in both materials. Finally, we disentangle the effects of adsorbate interactions on state coverages and kinetics to show how adsorbate interactions determine the observed Tafel slopes. Crucially, the case of CoFe-PB shows that, even where interactions are weaker, adsorption remains non-Nernstian, which strongly influences the observed Tafel slope.

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Structures of the intermediates of Kok's photosynthetic water oxidation clock.

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Structures of the intermediates of Kok's photosynthetic water oxidation clock.

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