During dark adaptation, a change in the 02-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 electron paramagnetic resonance (EPR) spectroscopy and 02 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 °C) and short-term (6 min at 0 °C) dark-adapted PSII membranes or thylakoids. The optimal temperature for producing this EPR signal in long-term dark-adapted samples is 200 K compared to 170 K for short-term dark-adapted samples. However, in short-term dark-adapted samples, illumination at 170 K produces an EPR signal with a different hyperfine structure and a wider field range than does illumination at 160 K or below. In contrast, 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 02 consumption activity of PSII or thylakoid membranes. PSII membranes and thylakoid membranes slowly consume 02 following illumination, but only when a functional OEC and excess reductant are present. We assign this slow consumption of 02 to a catalytic reduction of 02 by the OEC in the dark. The rate of 02 consumption decreases during dark adaptation; long-term dark-adapted PSII or thylakoid membranes do not consume 02 despite the presence of excess reductant. The EPR-detected change in the Mn site of the OEC and the decline of the 02 consumption activity observed in PSII or thylakoid membranes occur with the same time constant. It is proposed that 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, 02-consuming state to a resting state incapable of 02 consumption.
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