An Oscillating Manganese Electron Paramagnetic Resonance Signal from the S₀ State of the Oxygen Evolving Complex in Photosystem II

Abstract

Photosynthesis produces the oxygen necessary for all aerobic life. During this process, the manganese-containing oxygen evolving complex (OEC) in photosystem II (PSII), cycles through five oxidation states, S0-S4. One of these, S2, is known to be paramagnetic and gives rise to electron paramagnetic resonance (EPR) signals used to probe the catalytic structure and function of the OEC. The S0 states has long been thought to be paramagnetic. We report here a Mn EPR signal from the previously EPR invisible S0 state. The new signal oscillates with a period of four, indicating that it originates from fully active PSII centers. Although similar to the S2 state multiline signal, the new signal is wider (2200 gauss compared with 1850 gauss in samples produced by flashing), with different peak intensity and separation (82 gauss compared with 89 gauss). These characteristics are consistent with the S0 state EPR signal arising from a coupled MnII-MnIII intermediate. The new signal is more stable than the S2 state signal and its decay in tens of minutes is indicative of it originating from the S0 state. The S0 state signal will provide invaluable information toward the understanding of oxygen evolution in plants.

Stoichiometry of Proton Release from the Catalytic Center in Photosynthetic Water Oxidation

“…Only a manganese dimer was considered to be functional. The mixed valence states in S 0 and S 2 (spin ϭ 1 ⁄2) are in agreement with an EPR multiline signal in S 0 (41,42) and S 2 (43). Valence states of the manganeses have also been derived from x-ray absorption shifts at the manganese-K-edge (37-40) indicating manganese oxidations up to S 3 .…”

Absence of Mn-Centered Oxidation in the S2→ S3Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

“…Other spectroscopic studies 22,[25][26][27][34][35][36][37][38][39] concur that Mn oxidation occurs during the S 0 → S 1 transition. In addition, one possible explanation of the greater spectral width of the S 0 -state EPR multiline signal compared to the S 2 -state EPR multiline signal is that Mn(II) is present in the S 0 state, [25][26][27] which suggests a Mn(II) → Mn(III) oxidation for the S 0 → S 1 transition.…”

Investigation of the interaction of the water oxidising manganese complex of photosystem II with the aqueous solvent environment

“…The intensity of the S 2 multiline signal is increased by the addition of alcohols, the S 0 multiline signal is only observed in the presence of methanol [9,10]. These observations suggest that there may be a speci¢c interaction of methanol with the Mn complex and that investigation of this interaction may provide information both about the exposure of the Mn complex to the environment and possible substrate binding sites on the Mn complex.…”