Substrate Water Exchange for the Oxygen Evolving Complex in PSII in the S₁, S₂, and S₃ States

Abstract

Detailed mechanisms for substrate water exchange in the oxygen evolving complex in photosystem II have been determined with DFT methods for large models. Existing interpretations of the experimental water exchange results have been quite different. By many groups, these results have been the main argument against the water oxidation mechanism suggested by DFT, in which the oxygen molecule is formed between a bridging oxo and an oxyl radical ligand in the center of the OEC. That mechanism is otherwise in line with most experiments. The problem has been that the mechanism requires a rather fast exchange of a bridging oxo ligand, which is not a common finding for smaller Mn-containing model systems. However, other groups have actually favored a substrate derived oxo ligand partly based on the same experiments. In the present study, three S-states have been studied, and the rates have been well reproduced by the calculations. The surprising experimental finding that water exchange in S1 is slower than the one in S2 is reproduced and explained. The key to this rate difference is the ease by which one of the manganese centers (Mn3) is reduced. This reduction has to occur to release the substrate water from Mn3. The similar rate of the slow exchange in S2 and S3 has been rationalized on the basis of earlier experiments combined with the present calculations. The results strongly support the previous DFT-suggested water oxidation mechanism.

Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II

“…In this model, the Mn cluster is in the open cube configuration (O5 bound to dangler Mn4), and radical coupling was proposed to occur between the O5 oxo and an oxyl radical that forms after deprotonation of a hydroxide on the proximal Mn1. This model is consistent with the recent S (28,41,55,56), this alternative, therefore, also fits with this conclusion that critical water rearrangements, perhaps coupled to structural rearrangements, precede the dioxygen chemistry.…”

Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser

“…The increase in distance could allow for the binding of the second substrate water molecule between the dangler Mn and the Mn 3 CaO x cubane. The presence of a substrate water molecule between the dangler Mn and the distorted cubane in the higher S-states, has also been predicted to be essential for the catalytic mechanism in a recent DFT model of the full catalytic S-state cycle, including modelling of the substrate water exchange 21,53 . In addition to the elongation, the overall dimensions of the Mn 4 CaO 5 cluster appear to condense in the double-flash data set that may represent the putative S 3 -state.…”

Momentum-dependent band spin splitting in semiconducting MnO2: a density functional calculation

“…One is from an electronic structural point of view; the difficulty exists in the spin state of the catalyst, accelerating a reaction where two water molecules (reactants) of singlet spin states produce one oxygen molecule (products) of triplet spin states. The other is from a precise geometrical structural point of view; the difficulty lies in the fact that the OEC structure is known only for a dark-stable S 1 state, [11][12][13][14] although the OEC catalytic cycle consists of at least four states. 7,10,15 When it comes to the oxygen-evolution reaction by water splitting, in most of the artificial electrodes, precious metals such as platinum, ruthenium, and iridium are often indispensable, 16,17 owing to their durability.…”