Temperature dependence of the high-spin S₂ to S₃ transition in Photosystem II: Mechanistic consequences

The Mn₄CaO₅-cluster in Photosystem II advances through five oxidation states, S₀ to S₄, before water is oxidized and O₂ is generated. The S₂-state exhibits either a low-spin, S = 1/2 (S₂^LS), or a high-spin state, S = 5/2 (S₂^HS). Increasing the pH favors the S₂^HS configuration and mimics the formation of Tyr_Z in the S₂^LS-state at lower pH values (Boussac et al. Biochim. Biophys. Acta 1859 (2018) 342). Here, the temperature dependence of the S₂^HS to S₃ transition was studied by EPR spectroscopy at pH 8.6. The present data strengthened the involvement of S₂^HS as a transient state in the S₂^LSTyr_Z → S₂^HSTyr_Z → S₃Tyr_Z transition. Depending on the temperature, the S₂^HS progresses to S₃ states exhibiting different EPR properties. One S₃-state with a S = 3 signal, supposed to have a structure with the water molecule normally inserted in S₂ to S₃ transition, can be formed at temperatures as low as 77 K. This suggests that this water molecule is already bound in the S₂^HS state at pH 8.6. The nature of the EPR invisible S₃ state, formed down to 4.2 K from a S₂^HS state, and that of the EPR detectable S₃ state formed down to 77 K are discussed. It is proposed that in the S₂^LS to S₃ transition, at pH < 8.6, the proton release (Sugiura et al. Biochim. Biophys. Acta 1859 (2018) 1259), the S₂^LS to S₂^HS conversion and the binding of the water molecule are all triggered by the formation of Tyr_Z.