The in-depth understanding of the molecular mechanisms regulating the water oxidation catalysis is of key relevance for the rationalization and the design of efficient oxygen evolution catalysts based on earth-abundant transition metals. Performing ab initio DFT+U molecular dynamics calculations of cluster models in explicit water solution, we provide insight into the pathways for oxygen evolution of a cobalt-based catalyst (CoCat). The fast motion of protons at the CoCat/ water interface and the occurrence of cubane-like Co-oxo units at the catalyst boundaries are the keys to unlock the fast formation of O-O bonds. Along the resulting pathways, we identified the formation of Co(IV)-oxyl species as the driving ingredient for the activation of the catalytic mechanism, followed by their geminal coupling with O atoms coordinated by the same Co. Concurrent nucleophilic attack of water molecules coming directly from the water solution is discouraged by high activation barriers. The achieved results suggest also interesting similarities between the CoCat and the Mn 4 Ca-oxo oxygen evolving complex of photosystem II.
# These authors contributed equally to this work. Keywords ab initio calculations; density functional calculations; Kok cycle; photosystem II; water splittingOne of the key steps in photosynthetic solar-energy conversion performed by plants, algae, and cyanobacteria is the splitting of water into molecular oxygen and hydrogen equivalents. [1] To achieve this challenging task photosynthetic organisms use a protein complex that remained almost unchanged during the evolution in the last two and a half billion years: the photosystem II (PSII). The reaction proceeds by the accumulation of four oxidizing equivalents on the {Mn 4 CaO 5 } cluster through five (S 0 -S 4 ) oxidation states that are sequentially attained during water splitting (Kok cycle). [2] The deep understanding of the way nature has found to perform this difficult task efficiently has a great relevance not only for biology but also for inspiring the development of biomimetic artificial systems that can be used to store solar energy in an environmentally friendly way. [3] Atomic details of the structure of the oxygen-evolving complex (OEC) of PSII have been revealed by extended Xray absorption fine structure (EXAFS) experiments and by X-ray crystallography at increasing resolution levels. [4] However, the accurate position of the {Mn 4 CaO 5 } cluster atoms and its ligands emerged only when a X-ray structure at 1.9 Å resolution became accessible. [5] However, the effect of a possible X-ray photo-reduction, in particular on the characterization of the Kok's state described by this structure and on the unrealistic bond lengths between the oxygen atom O5 and the two manganese ions Mn1 and Mn4, is matter of debate. [6] Additionally, important contributions to the structure refinement came from theoretical studies. [6b,7] Apart from a detailed characterization of the molecular structure of the OEC, an exact description of the water-splitting catalytic mechanism cannot leave aside an accurate
Water oxidation in photosynthetic organisms occurs through the five intermediate steps S 0 -S 4 of the Kok cycle in the oxygen evolving complex of photosystem II (PSII). Along the catalytic cycle, four electrons are subsequently removed from the Mn 4 CaO 5 core by the nearby tyrosine Tyr-Z, which is in turn oxidized by the chlorophyll special pair P680, the photo-induced primary donor in PSII. Recently, two Mn 4 CaO 5 conformations, consistent with the S 2 state (namely, S A 2 and S B 2 models) were suggested to exist, perhaps playing a different role within the S 2 -to-S 3 transition. Here we report multiscale ab initio density functional theory plus U simulations revealing that upon such oxidation the relative thermodynamic stability of the two previously proposed geometries is reversed, the S B 2 state becoming the leading conformation. In this latter state a proton coupled electron transfer is spontaneously observed at ∼100 fs at room temperature dynamics. Upon oxidation, the Mn cluster, which is tightly electronically coupled along dynamics to the Tyr-Z tyrosyl group, releases a proton from the nearby W1 water molecule to the close Asp-61 on the femtosecond timescale, thus undergoing a conformational transition increasing the available space for the subsequent coordination of an additional water molecule. The results can help to rationalize previous spectroscopic experiments and confirm, for the first time to our knowledge, that the water-splitting reaction has to proceed through the S B 2 conformation, providing the basis for a structural model of the S 3 state.QM/MM | photosynthesis | molecular dynamics | reaction mechanisms F or 2.5 Gy photosynthetic organisms have used the photosystem II complex (PSII) to capture light energy from the sun and convert it into chemical energy stored within energy-rich carbohydrates (1). The water oxidation reaction, occurring in the reaction center of PSII, represents the central step of the natural photosynthetic process, leading to the formation of molecular oxygen and hydrogen equivalents. A deep understanding of the photosynthetic water-splitting mechanism may serve as a valuable source of inspiration for the development of artificial devices able to store solar energy in environmentally friendly fuels, such as molecular hydrogen (2-6). The active site of the PSII enzyme, where the water-splitting reaction takes place, consists of a core of four Mn ions and one Ca ion connected together through μ-oxo bridges in a cubane-like aggregate (7). Water oxidation proceeds through five sequential S 0 ÀS 4 steps known as the Kok cycle (8). At each step of the catalytic cycle the absorption of photons turns out the oxidation of the tyrosyl group of a nearby tyrosine (i.e., Tyr161, also known as Tyr-Z in the D1 subunit of PSII), which acts as an intermediate in the electron transfer between the Mn 4 CaO 5 cluster and the primary donor P680 (9, 10).The molecular structure for the different states of the Kok cycle was largely investigated in the past decades by extended X-ray absor...
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