pH dependence of photosystem II photoinhibition: relationship with structural transition of oxygen-evolving complex at the pH of thylakoid lumen.

Ca-depleted photosystem II membranes (PSII[-Ca]) do not contain PsbP and PsbQ proteins protecting the Mn4CaO5 cluster of the PSII oxygen-evolving complex (OEC). Therefore, the Mn ions in the PSII(-Ca) membranes can be reduced by exogenous bulky reductants or the charged reductant Fe(II). We have recently found that the resistance of Mn ions in the OEC to the Fe(II) action is pH dependent and that this reductant is less effective at pH 5.7 than at pH 6.5 (Semin et al. J Photochem Photobiol B 178:192, 2018). Taking these data into account, we investigated the photoinhibition in different PSII membranes at pH 5.7 and 6.5 and found that the resistance to photoinhibition of PSII and PSII(-Ca) membranes with a Mn cluster is higher at pH 5.7 than at pH 6.5, whereas the resistance of the Mn-depleted PSII membranes is pH independent. In thylakoids, light generates the transmembrane ΔpH, leading to the acidulation of lumen that results in pH 5.7. The uncouplers (NH4Cl or nigericin) that significantly prevent acidulation increase the rate of PSII photoinhibition in thylakoids. We suggest that the structural transition in the OEC at pH 5.7 plays a role of a built-in mechanism increasing the resistance of OEC to photoinhibition under illumination, since it is accompanied by a pH decrease in lumen to 5.7. The coincidence of these pH values, i.e. lumen pH under illumination and pH of the maximal resistance of the Mn cluster to the reduction by reductants, can point at the pH-dependent mechanism of PSII self-protection from photoinactivation.