Temperature dependence of the high-spin S to S transition in Photosystem II: Mechanistic consequences.

The MnCaO-cluster in Photosystem II advances through five oxidation states, S to S, before water is oxidized and O is generated. The S-state exhibits either a low-spin, S = 1/2 (S), or a high-spin state, S = 5/2 (S). Increasing the pH favors the S configuration and mimics the formation of Tyr in the S-state at lower pH values (Boussac et al. Biochim. Biophys. Acta 1859 (2018) 342). Here, the temperature dependence of the S to S transition was studied by EPR spectroscopy at pH 8.6. The present data strengthened the involvement of S as a transient state in the STyr → STyr → STyr transition. Depending on the temperature, the S progresses to S states exhibiting different EPR properties. One S-state with a S = 3 signal, supposed to have a structure with the water molecule normally inserted in S to S transition, can be formed at temperatures as low as 77 K. This suggests that this water molecule is already bound in the S state at pH 8.6. The nature of the EPR invisible S state, formed down to 4.2 K from a S state, and that of the EPR detectable S state formed down to 77 K are discussed. It is proposed that in the S to S transition, at pH < 8.6, the proton release (Sugiura et al. Biochim. Biophys. Acta 1859 (2018) 1259), the S to S conversion and the binding of the water molecule are all triggered by the formation of Tyr.