•Catalytic reactions of oxygen-evolving complex during the S2→S3 transition are investigated.•Two reaction pathways, R- and L-reactions are elucidated.•Both reactions start by moving the Ca-bound ...water (W3) to the vacant Mn(III) coordination.•The L-reaction is more energetically favored than the R-reaction.•Proton transfer occurs through O5, W2(OH) and the active site water molecules (W5–W7).
Catalytic reactions of the proton and electron transfers occurring at the oxygen-evolving complex (OEC) of photosystem II during the S2–S3 transition were investigated by the quantum mechanics/molecular mechanics (QM/MM) methodology. Two favorable reaction pathways were elucidated. Both reactions start by moving the Ca-bound water (W3) to the vacant Mn(III) coordination at the left-opened (L) or right-opened (R) form. The former reaction pathway, in which W3 coordinates to the Mn4 at the S2-L form, has lower activation barriers than the latter. Thus, easier proton transfers from W3 to the Tyr161 phenol anion can be performed.
Photosynthetic water oxidation is catalyzed by the Mn
CaO
cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S
to S
). To reveal the mechanism of water ...oxidation, we analyzed structures of PSII in the S
, S
, and S
states by x-ray free-electron laser serial crystallography. No insertion of water was found in S
, but flipping of D1 Glu
upon transition to S
leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn
CaO
cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reveal cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation.
We have performed hybrid density functional theory (DFT) calculations to investigate how chemical equilibria can be described in the S3 state of the oxygen-evolving complex in photosystem II. For a ...chosen 340-atom model, 1 stable and 11 metastable intermediates have been identified within the range of 13 kcal mol–1 that differ in protonation, charge, spin, and conformational states. The results imply that reversible interconversion of these intermediates gives rise to dynamic equilibria that involve processes with relocations of protons and electrons residing in the Mn4CaO5 cluster, as well as bound water ligands, with concomitant large changes in the cluster geometry. Such proton tautomerism and redox isomerism are responsible for reversible activation/deactivation processes of substrate oxygen species, through which Mn–O and O–O bonds are transiently ruptured and formed. These results may allow for a tentative interpretation of kinetic data on substrate water exchange on the order of seconds at room temperature, as measured by time-resolved mass spectrometry. The reliability of the hybrid DFT method for the multielectron redox reaction in such an intricate system is also addressed.
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•Effect of spin contamination on energies of solids was evaluated by DFT.•Spin contamination errors affect AFM state total energies.•Spin contamination error in solids was larger than ...that in molecular systems.•Estimating these errors is crucial for studying functional solid materials.•Effects of the errors varied by the on-site parameter used.
Estimation and the importance of spin contamination errors (SCEs) in theoretical calculations related to open-shell molecular systems are well known. However, there is no estimation scheme available for density functional theory (DFT)/plane-wave, a standard first-principles method for solid materials. Therefore, in this study, we established the estimation scheme of SCE in DFT/plane-wave using approximate spin projection, and the new scheme was applied to typical models with stable antiferromagnetic states to illustrate the importance of SCE correction in solid systems.
This review article describes a historical perspective of elucidation of the nature of the chemical bonds of the high-valent transition metal oxo (M=O) and peroxo (M-O-O) compounds in chemistry and ...biology. The basic concepts and theoretical backgrounds of the broken-symmetry (BS) method are revisited to explain orbital symmetry conservation and orbital symmetry breaking for the theoretical characterization of four different mechanisms of chemical reactions. Beyond BS methods using the natural orbitals (UNO) of the BS solutions, such as UNO CI (CC), are also revisited for the elucidation of the scope and applicability of the BS methods. Several chemical indices have been derived as the conceptual bridges between the BS and beyond BS methods. The BS molecular orbital models have been employed to explain the metal oxyl-radical character of the M=O and M-O-O bonds, which respond to their radical reactivity. The isolobal and isospin analogy between carbonyl oxide R2C-O-O and metal peroxide LFe-O-O has been applied to understand and explain the chameleonic chemical reactivity of these compounds. The isolobal and isospin analogy among Fe=O, O=O, and O have also provided the triplet atomic oxygen (3O) model for non-heme Fe(IV)=O species with strong radical reactivity. The chameleonic reactivity of the compounds I (Cpd I) and II (Cpd II) is also explained by this analogy. The early proposals obtained by these theoretical models have been examined based on recent computational results by hybrid DFT (UHDFT), DLPNO CCSD(T0), CASPT2, and UNO CI (CC) methods and quantum computing (QC).
Photosynthetic water oxidation is catalyzed by a Mn4CaO5-cluster in photosystem II through an S-state cycle. Understanding the roles of heterogeneity in each S-state, as identified recently by the ...EPR spectroscopy, is very important to gain a complete description of the catalytic mechanism. We performed herein hybrid DFT calculations within the broken-symmetry formalism and associated analyses of Heisenberg spin models to study the electronic and spin structures of various isomeric structural motifs (hydroxo–oxo, oxyl–oxo, peroxo, and superoxo species) in the S3 state. Our extensive study reveals several factors that affect the spin ground state: (1) (formal) Mn oxidation state; (2) metal–ligand covalency; (3) coordination geometry; and (4) structural change of the Mn cluster induced by alternations in Mn···Mn distances. Some combination of these effects could selectively stabilize/destabilize some spin states. We found that the high spin state (S total = 6) of the oxyl–oxo species can be causative for catalytic function, which manifests through mixing of the metal–ligand character in magnetic orbitals at relatively short O5···O6 distances (<2.0 Å) and long MnA···O5 distances (>2.0 Å). These results will serve as a basis to conceptually identify and rationalize the physicochemical synergisms that can be evoked by the unique “distorted chair” topology of the cluster through cooperative Jahn–Teller effects on multimetallic centers.
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•New O–O bond formation mechanism of photosystem II oxygen-evolving complex is proposed.•At least five reaction steps were required in the S4 to S0 transition.•Initial proton transfer ...requires a highest activation barrier among the five reaction steps.•O–O single bond is formed by a nonadiabatic one-electron transfer from the Mn cluster to Yz.•Proton transfer occurs to neutralize the Yz anion.
The reaction mechanism of the O2 formation in the S4 state of the oxygen-evolving complex of photosystem II was clarified at the quantum mechanics/molecular mechanics (QM/MM) level. After the Yz (Y161) oxidation and the following proton transfer in the S3 state, five reaction steps are required to produce the molecular dioxygen. The highest barrier step is the first proton transfer reaction (0 → 1). The following reactions involving electron transfers were precisely analyzed in terms of their energies, structures and spin densities. We found that the one-electron transfer from the Mn4Ca cluster to Y161 triggers the O–O sigma bond formation.
The O2 release of the oxygen-evolving complex of the photosystem II (PSII) is one of the essential processes responsible for the highly efficient O2 production. Despite its importance, the detailed ...molecular mechanism is still unsolved. In the present study, we show that the O2 release is directly coupled with water insertion into the Mn cluster based on the quantum mechanics/molecular mechanics (QM/MM) calculations. In this mechanism, the O2 molecule first dissociates from the Mn sites in order, that is, the O atom coordinating to the Mn3 (O5a) first dissociates, then the other O atom coordinating to the Mn1 (O5d) dissociates in the next step in the late S4 state (1 → 2). Next, the O2 migrates to a space surrounded by the Val185 and His332 side chains as one water molecule coordinating to the Ca2+ ion (W3) comes into the O2 bonded site (2 → 3). Finally, a pre-S0 state (4) is formed after a proton transfer from the inserted water to the other proton acceptor site (W2) (3 → 4). The highest activation barrier during these reactions was found at the O2 release step (2 → 3) that only requires E ⧧ = 12.7 kcal mol–1 (G ⧧ = 10.4 kcal mol–1). A series of the reactions (2 → 3) look like a chain crash of billiard balls because the W3 is inserted into the catalytic center from the water-abundant side (Ca2+ ion side), and then the O2 moiety is pushed out to the opposite side (Val185 side). The hydrophobic residue of Val185 covers the active O5 site and forms an O2-specific permeation tunnel. The present sequential reactions clearly demonstrate the efficient removal of the toxic O2 from the catalytic center and implications of the essential roles of Val185, Ca2+ ions and water molecules, which are all present in the active site of PSII as the indispensable constituents.
•Experimental results on the natural water oxidation catalyst are summarized.•Theoretical studies on the natural water oxidation catalyst are summarized and compared with the experimental ...results.•Comparisons between experimental and theoretical studies point to a unified mechanism for natural water oxidation.•The catalyst serves as a blueprint for artificial catalyst of water oxidation.
The aim of this review is to elucidate geometric structures of the catalytic CaMn4Ox (x = 5, 6) cluster in the Kok cycle for water oxidation in the oxygen evolving complex (OEC) of photosystem II (PSII) based on the high-resolution (HR) X-ray diffraction (XRD) and serial femtosecond crystallography (SFX) experiments using the X-ray free-electron laser (XFEL). Quantum mechanics (QM) and QM/molecular mechanics (MM) computations are performed to elucidate the electronic and spin structures of the CaMn4Ox (x = 5, 6) cluster in five states Si (i = 0 ∼ 4) on the basis of the X-ray spectroscopy, electron paramagnetic resonance (EPR) and related experiments. Interplay between the experiments and theoretical computations has been effective to elucidate the coordination structures of the CaMn4Ox (x = 5, 6) cluster ligated by amino acid residues of the protein matrix of PSII, valence states of the four Mn ions and total spin states by their exchange-couplings, and proton-shifted isomers of the CaMn4Ox (x = 5, 6) cluster. The HR XRD and SFX XFEL experiments have also elucidated the biomolecular systems structure of OEC of PSII and the hydrogen bonding networks consisting of water molecules, chloride anions, etc., for water inlet and proton release pathways in PSII. Large-scale QM/MM computations have been performed for elucidation of the hydrogen bonding distances and angles by adding invisible hydrogen atoms to the HR XRD structure. Full geometry optimizations by the QM and QM/MM methods have been effective for elucidation of the molecular systems structure around the CaMn4Ox (x = 5, 6) cluster in OEC. DLPNO-CCSD(T0) method has been applied to elucidate relative energies of possible intermediates in each state of the Kok cycle for water oxidation. Implications of these results are discussed in relation to the blueprint for developments of artificial catalysts for water oxidation.
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