X-ray absorption spectroscopy on layered photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S0-S1, S1-S2, and S2-S3 transitions of the water oxidation cycle

By application of microsecond light flashes the oxygen-evolving complex (OEC) was driven through its functional cycle, the S-state cycle. The S-state population distribution obtained by the application of n flashes (n = 0 ... 6) was determined by analysis of EPR spectra; Mn K-edge X-ray absorption spectra were collected. Taking into consideration the likely statistical error in the data and the variability stemming from the use of three different approaches for the determination of edge positions, we obtained an upshift of the edge position by 0.8-1.5, 0.5-0.9, and 0.6-1.3 eV for the S-0-S-1, S-1-S-2, and S-2-S-3 transitions, respectively, and a downshift by 2.3-3.1 eV for the S-3-S-0 transition. These results are highly suggestive of Mn oxidation state changes for all four S-state transitions. In the So-state spectrum, a clearly resolved shoulder in the X-ray spectrum around 6555 eV points toward the presence of Mn(II). We propose that photosynthetic oxygen evolution involves cycling of the photosystem II manganese complex through four distinct oxidation states of this tetranuclear complex: Mn(II)-Mn(III) -Mn(IV)(2) in the So-state, Mn(III)(2)-Mn(IV)(2) in the S-1-state, Mn(III)(1)-Mn(IV)(3) in the S-2-state, and Mn(IV)(4) in the S-3-state.