Active and resting states of the oxygen-evolving complex of photosystem II

Abstract

During dark adaptation, a change in the O2-evolving complex (OEC) of spinach photosystem II (PSII) occurs that affects both the structure of the Mn site and the chemical properties of the OEC, as determined from low-temperature EPR spectroscopy and O2 measurements. The S2-state multiline EPR signal, arising from a Mn-containing species in the OEC, exhibits different properties in long-term (4 h at 0.degree. C) and short-term (6 min at 0.degree. C) dark-adapted PSII membranes or thylakoids. The optimal temperature for producing this EPR signal in long-term dark-adapted samples is 200.degree. K compared to 170.degree. K for short-term dark-adapted samples. However, in short-term dark-adapted samples, illumination at 170.degree. K produces an EPR signal with a different hyperfine structure and a wider field range than does illumination at .ltoreq. 160.degree. K. The line shape of the S2-state EPR signal produced in long-term dark-adapted samples is independent of the illumination temperature. The EPR detected change in the Mn site of the OEC that occurs during dark adaptation is correlated with a change in O2 consumption activity of PSII or thylakoid membranes. PSII membranes and thylakoid membranes slowly consume O2 following illumination, but only when a functional OEC and excess reductant are present. This slow consumption of O2 is assigned to a catalytic reduction of O2 by the OEC in the dark. The rate of O2 consumption decreases during dark adaptation; long-term dark-adapted PSII or thylakoid membranes do not consume O2 despite the presence of excess reductant. The EPR-detected change in the Mn site of the OEC and the decline of the O2 consumption activity observed in PSII or thylakoid membranes occur with the same time constant. Evidently, a structural change in the Mn site of the OEC occurs during dark adaptation, changing the electron-transport properties of the donor side of PSII and causing a conversion from an active, O2-consuming state to a resting stage incapable of O2 consumption.