In photosystem II (PSII), water oxidation occurs in the Mn 4 CaO 5 cluster with the release of electrons via the redox-active tyrosine (TyrZ) to the reaction-center chlorophylls (P D1 /P D2 ). Using a quantum mechanical/molecular mechanical approach, we report the redox potentials (E m ) of these cofactors in the PSII protein environment. The E m values suggest that the Mn 4 CaO 5 cluster, TyrZ, and P D1 /P D2 form a downhill electron transfer pathway. E m for the first oxidation step, E m (S 0 /S 1 ), is uniquely low (730 mV) and is ∼100 mV lower than that for the second oxidation step, E m (S 1 /S 2 ) (830 mV) only when the O4 site of the Mn 4 CaO 5 cluster is protonated in S 0 . The O4-water chain, which directly forms a low-barrier H-bond with the Mn 4 CaO 5 cluster and mediates protoncoupled electron transfer in the S 0 to S 1 transition, explains why the second lowest oxidation state, S 1 , is the most stable and S 0 is converted to S 1 even in the dark.

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In photosystem II, water oxidation occurs at the oxygen-evolving complex (OEC). The presence of a hydronium ion (H 3 O + ) was proposed at the Cl − binding site and Ca 2+ -depleted OEC. Using a quantum mechanical/molecular mechanical approach, we report the stability of H 3 O + in the PSII protein environment. Neither release of the proton from ligand water molecule W2 at the OEC nor formation of H 3 O + at Cl − is energetically favorable. In contrast, H 3 O + can exist at the Ca 2+ -depleted OEC. Even when H 3 O + exists in Ca 2+ -depleted PSII, the H-bond network of the redox-active tyrosine (TyrZ) remains unaltered, retaining the unusually short low-barrier H-bond with D1-His190, and the redox potential of TyrZ, E m (TyrZ), remains unaltered. These observations explain why the oxidation of the Ca 2+ -depleted Mn 4 O 5 cluster by TyrZ (i.e., the S 2 to S 3 transition) is not inhibited at low pH. It seems likely that Ca 2+ plays a role in not only (i) maintaining the H-bond network and facilitating TyrZ oxidation [tuning E m (TyrZ)] but also (ii) providing the valence of +2, decreasing the pK a of the ligand molecule (W1), and facilitating the release of the proton from W1 in the S 2 to S 3 transition together with Cl − . Article pubs.acs.org/biochemistry

Low-barrier H-bonds form when the pKa values of the H-bond donor and acceptor moieties are nearly equal. Here, we report redox potential (Em) values along two redox-active low-barrier H-bonds in...

The O···O distance for a typical H-bond is ∼2.8 Å, whereas the radiation-damage-free structures of photosystem II (PSII), obtained using the X-ray free electron laser (XFEL), shows remarkably short O···O distances of ∼2 Å in the oxygen-evolving Mn4CaO5/6 complex. Herein, we report the protonation/oxidation states of the short O···O atoms in the XFEL structures using a quantum mechanical/molecular mechanical approach. The O5···O6 distance of 1.9 Å is reproduced only when O6 is an unprotonated O radical (O•–) with Mn­(IV)3Mn­(III), i.e., the S3 state. The potential energy profile shows a barrier-less energy minimum region when O5···O6 = 1.90–2.05 Å (O•– ↓) or 2.05–2.20 Å (O•– ↑). Formation of such a short O5···O6 distance is not possible when O6 is OH– with Mn­(IV)4. In the case in which the O5···O6 distance is 1.9 Å, it seems likely that the O radical species exists in the oxygen-evolving complex of the XFEL-S3 crystals.