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

Abstract

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 S0-S1, S1-S2, and S2-S3 transitions, respectively, and a downshift by 2.3-3.1 eV for the S3-S0 transition. These results are highly suggestive of Mn oxidation state changes for all four S-state transitions. In the S0-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 S0-state, Mn(III)2-Mn(IV)2 in the S1-state, Mn(III)1-Mn(IV)3 in the S2-state, and Mn(IV)4 in the S3-state.

Simulation of the isotropic EXAFS spectra for the S 2 and S 3 structures of the oxygen evolving complex in photosystem II

“…This change, supported by results of earlier and later XANES spectra (33), led to the conclusion that an oxygen rather than a manganese is oxidized in this transition, which strongly affected the suggested O-O bond formation mechanism (34,35). The conclusion from the XANES spectra has been questioned experimentally (36), and also recently on the basis of DFT model calculations (37). The Dau and coworkers results, however, gave one change from a distance larger than 3.0 Å down to 2.77 Å; this led to a suggested structural change in this transition with a formation of an additional Mn-Mn bis-μ-oxo bridge in S 3 (38).…”

Eukaryotically Encoded and Chloroplast-located Rubredoxin Is Associated with Photosystem II

“…PSII-enriched membrane fragments were prepared as described previously (13). The protocol for the preparation of n-octyl-␤-D-glycosidesolubilized PSII core particles ("OG cores") and PSII core dimers described by Hankamer et al (14) was modified in that the osmoprotective agent glycine betaine (GlyB) was used throughout the preparation.…”

Structural Change of the Mn Cluster during the S2→S3 State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

“…However, on the basis of Mn K-edge studies, other groups have proposed that Mn is oxidized during the S 0 →S 1 , S 1 →S 2 , and also during the S 2 →S 3 transitions. 17,18 The requirement of a higher signal-to-noise ratio for the EXAFS relative to the XANES experiments has made EXAFS measurements more difficult for the flash-induced S state samples. Earlier EXAFS data from the chemically treated S 3 state samples produced by a double-turnover method indicated that the two di-μ-oxo-bridged Mn-Mn dimer units may become nonequivalent.…”