Structural evidence for intermediates during O2 formation in photosystem II

Abstract

In natural photosynthesis, the light-driven splitting of water into electrons, protons and molecular oxygen forms the first step of the solar-to-chemical energy conversion process. The reaction takes place in photosystem II, where the Mn4CaO5 cluster first stores four oxidizing equivalents, the S0 to S4 intermediate states in the Kok cycle, sequentially generated by photochemical charge separations in the reaction center and then catalyzes the O–O bond formation chemistry1–3. Here, we report room temperature snapshots by serial femtosecond X-ray crystallography to provide structural insights into the final reaction step of Kok’s photosynthetic water oxidation cycle, the S3→[S4]→S0 transition where O2 is formed and Kok’s water oxidation clock is reset. Our data reveal a complex sequence of events, which occur over micro- to milliseconds, comprising changes at the Mn4CaO5 cluster, its ligands and water pathways as well as controlled proton release through the hydrogen-bonding network of the Cl1 channel. Importantly, the extra O atom Ox, which was introduced as a bridging ligand between Ca and Mn1 during the S2→S3 transition4–6, disappears or relocates in parallel with Yz reduction starting at approximately 700 μs after the third flash. The onset of O2 evolution, as indicated by the shortening of the Mn1–Mn4 distance, occurs at around 1,200 μs, signifying the presence of a reduced intermediate, possibly a bound peroxide.

Decoding Natural Strategy: Oxygen-Evolution Reaction on the Surface of Nickel Oxyhydroxide at Extremely Low Overpotential

“…Thinking outside the box strategies, such as ultrasound and magnetic field-assisted water splitting, are promising in the OER field. , In Nature, cyanobacteria, algae, and plants utilize a similar oxygen-evolving complex (OEC). − This biocatalyst is situated in Photosystem II, a membrane-protein complex that functions as a light-driven water oxidase in oxygenic photosynthesis. − The biological OEC, an Mn–Ca cluster, oxidizes water with a notably low overpotential (20 mV) and a high turnover frequency, releasing 25–90 molecules of O 2 per second. , According to a mechanism widely accepted by Kok, OEC can exist in five states (S 0 to S 4 ) postcharge accumulation based on Mn­(III)/Mn­(IV). The system progresses from the most reduced state, S 0 , to the most oxidized state, S 4 , as photons are captured by photosystem II. , The unstable S 4 state reacts with water to produce O 2 .…”

Nature of S-States in the Oxygen-Evolving Complex Resolved by High-Energy Resolution Fluorescence Detected X-ray Absorption Spectroscopy

“…By combining high-resolution XAS data with QM calculations, we have clearly shown that recent controversies regarding the nature of the S 3 state can be rigorously resolved and that presence of either peroxo or oxo/oxyl level intermediate can be ruled out. An all-Mn(IV) S 3 state should be considered as the starting intermediate in the interpretation of experimental data on the S 3 to S 0 transition. , Overall, the results of this work clearly show Mn-based oxidation during the S 2 to S 3 transition and constrain the possible mechanisms of the formation of the O–O bond to those that initiate after the final light-driven oxidation. Beyond the importance for biological water oxidation, the cumulative metal-centered storage of oxidizing equivalents supported by the present study directs our attention to synthetic water oxidation catalysts that leverage multimetallic cooperativity.…”

Engineering a molecular ruthenium catalyst into three-dimensional metal covalent organic frameworks for efficient water oxidation

“…Of note is that, in the natural photosystem II (PS II), the water oxidation occurs through first storing four oxidizing equivalents into the oxygen-evolving complex (OEC) featuring the Mn 4 CaO 5 reaction center and then catalyzing the O–O bond formation. 9–11 Inspired by the OEC in PS II, great efforts have been devoted to the investigation of molecular and supramolecular WOCs being structurally and functionally analogous to the Mn 4 CaO 5 cluster. 12–16…”