Considerations on the mechanism of photosynthetic water oxidation – dual role of oxo-bridges between Mn ions in (i) redox-potential maintenance and (ii) proton abstraction from substrate water

Abstract

Two mechanistic problems of photosynthetic water oxidation at the Mn complex of Photosystem II (PS II) are considered. (I) In the four Mn-oxidizing transitions, any pure Mn oxidation is predicted to cause an increase in redox potential that renders subsequent oxidation steps impossible (redox-potential problem). Formation of unprotonated oxo-bridges may counteract the potential increase. (II) The O-O formation step without any high-pK bases acting as proton acceptors is energetically unfavorable (acceptor-base problem). The pK of oxides in a bridging position between Mn ions may increase drastically upon reduction of Mn in the water-oxidation step (>10 units), thus rendering them favorable proton acceptors. It is proposed that in PS II, in the course of the four oxidizing transitions at least two unprotonated oxo-bridges are formed. Thereby (i) a redox potential increase is prevented and (ii) proton acceptors are prepared for the O-O formation step. Water oxidation in the O-O bond formation step is facilitated by simultaneous Mn reduction and proton transfer to bridging oxides amounting to hydrogen atom or hydride transfer from substrate water to the Mn-oxo core of the Mn complex of PS II.

Rapid Loss of Structural Motifs in the Manganese Complex of Oxygenic Photosynthesis by X-ray Irradiation at 10–300 K

“…In S 1 it is highly positive; approximately ϩ1 V (41). A potential increase upon the S 1 3 S 2 transition and a decrease in the S 0 * state is anticipated (41,42); the potential of the Mn II 4 state presumably is comparably low (Յ0 V) (43,44). That electrophilic centers are the primary target for reduction by electrons liberated because of x-ray exposure is also supported by investigations on protein crystals where disulfide bridges first became reduced at 100 K (18,19) and by EPR results (Ref.…”

“…Thus, the native S 0 as created by light flash application at room temperature may contain one Mn(-O) 2 Mn and one Mn(-O)(-OH)Mn unit (4,7). At room temperature the S 0 3 S 1 transition is electroneutral (65,66); probably the manganese oxidation is coupled to deprotonation of a -OH bridge (7,36,42). At the cryogenic temperatures where the S 1 3 S 0 * step occurred, charge-compensating long-range proton movements are unlikely so that protonation is impaired, and instead the -O bridge is broken.…”

Surface modification of hematite photoanode films with rhodium

“…All these factors are beneficial for improving the photocurrents. In this composite photoanode, photon absorption and redox catalysis are separated, which is similar to the photosystem II [21].…”

Water Oxidation by Co‐Based Oxides with Molecular Properties

“…[92] previously concluded that O(H)-bridged metal centers are a candidate for a common structural motif in multinuclear WOCs. The O(H) bridges may have an essential role in reducing the overpotential for water oxidation by redox-potential leveling; that is, the maintenance of an approximately constant redox potential for the four sequential oxidation steps assumed to occur before O 2 formation, as discussed in more detail in reference [93][94][95]. This redox leveling could be facilitated on the atomic scale by coupling of -OH deprotonation to the oxidation step, possibly in close analogy to processes in PSII [91].…”