Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn₄O₅ cluster of PSII refined to 1.9 Å X‐ray resolution

Abstract

Recently, Umena et al. have revealed the X-ray diffraction structure of the CaMn 4 O 5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) refined to 1.9 Å resolution. Their X-ray structure has first elucidated hydrogen-bonding networks and proton release pathways at OEC of PSII. Here, several working hypotheses Additional Supporting Information may be found in the online version of this article Correspondence to: S. Yamanaka; e-mail: syama@chem.sci.osaka-u.ac.jp Contract grant sponsor: Grants-in-Aid for Scientific Research; Contract grant numbers: 19750046, 19350070, 18350008, 23550016 (heuristic principles) for water splitting reaction are derived from their X-ray structure for theoretical modeling. These hypotheses suggest how water can be oxidized at OEC of PSII: namely possible reaction mechanisms for the reaction. To confirm them, we have also performed broken-symmetry (BS) UB3LYP calculations for active site models based on their XRD structure. The bond lengths of formal Mn(V)AO with labile dp-pp bonds are optimized to clarify possible roles of the species that are often introduced as a key intermediate in the catalytic (Kok) cycle for water splitting reaction at OEC of PSII. Location of the transition structure for the oxygen-oxygen (OAO) bond formation is also performed by the energy optimization technique. The natural orbital (NO) analysis of the UB3LYP solutions has been performed to obtain the natural molecular orbitals and their occupation numbers that have been useful for classification of localized d-electrons, labile chemical bonds and closed-shell (valence) orbitals. The localized d-electrons characterized by the NO analysis are the origins for the magnetism revealed by ENDOR and other magnetic experiments. On the other hand, the nature of labile (soft) dp-pp bonds responsible for the OAO bond formation has been investigated on the basis of chemical indices such as effective bond order (b), diradical character (y), and spin density (Q) indices that are calculated using the orbital overlap between broken-symmetry orbitals. These chemical indices have been calculated for the transition structure of the OAO bond formation at OEC of PSII. Implications of present computational results are discussed in relation to the derived hypotheses and available accumulated experimental results.

Similarities of artificial photosystems by ruthenium oxo complexes and native water splitting systems

“…We can determine the quantum corrections using the (S t 2 ) values by the UB3LYP calculations as shown in SI Text. Table 2 summarizes the quantum-corrected J values after the approximate spin projection (AP) that eliminates the spin contamination in the BS solution (7)(8)(9)(10). The AP correction is not negligible for the AF exchange integrals, J ab and J cd , because the size of local spin is 1∕2 in 2bb and 2a(+)ee.…”

“…However, as shown in the previous natural orbital analysis of BS solutions for 3, the magnetic local spins in three t 2g orbitals of each Mn(X) (X ¼ III, IV) ions are almost intact for the O─O bond formation. This means that local spin (s ¼ 1∕2) in the e g orbital of the Mn ion plays an important role for formation of the labile Mn-O bond (7)(8)(9)(10), indicating the similarity between 2bb and 3.…”

“…Eight different electronic and spin structures are calculated for tetraradical intermediates generated in the course of water splitting reaction by 2. The Heisenberg spin Hamiltonian model for the species is derived to elucidate six different effective exchange interactions (J) for four spin systems (7)(8)(9)(10). Six J values are determined using total energies of the eight (or seven) BS solutions for different spin configurations.…”

Detection of an intermediary, protonated water cluster in photosynthetic oxygen evolution

“…In another approach, the recombination kinetics of YZ• were used as a probe of electrostatic changes in the network in the S 2 and S 0 states (21, 22). In both studies, ammonia, a substrate-based inhibitor (23-25), was used to perturb hydrogen bonding in the OEC and was shown to have significant effects on the spectroscopic signals (18,20,22).Proton-coupled electron-transfer reactions occur during the S-state cycle (11,12). Although the S 1 -to-S 2 transition is not accompanied by a net proton release to sucrose-containing buffers, proton release accompanies the other S-state transitions (26).…”

“…Proton-coupled electron-transfer reactions occur during the S-state cycle (11,12). Although the S 1 -to-S 2 transition is not accompanied by a net proton release to sucrose-containing buffers, proton release accompanies the other S-state transitions (26).…”