Comparison of the Manganese Cluster in Oxygen-Evolving Photosystem II with Distorted Cubane Manganese Compounds through X-ray Absorption Spectroscopy

Abstract

X-ray absorption spectroscopy has been employed to assess the degree of similarity between the oxygen-evolving complex (OEC) in photosystem II (PS II) and a family of synthetic manganese complexes containing the distorted cubane [Mn(4)O(3)X] core (X = benzoate, acetate, methoxide, hydroxide, azide, fluoride, chloride, or bromide). These [Mn(4)(&mgr;(3)-O)(3)(&mgr;(3)-X)] cubanes possess C(3)(v)() symmetry except for the X = benzoate species, which is slightly more distorted with only C(s)() symmetry. In addition, Mn(4)O(3)Cl complexes containing three or six terminal Cl ligands at three of the Mn were included in this study. The Mn K-edge X-ray absorption near edge structure (XANES) from the oxygen-ligated complexes begin to resemble general features of the PS II (S(1) state) spectrum, although the second derivatives are distinct from those in PS II. The extended X-ray absorption fine structure (EXAFS) of these Mn compounds also displays superficial resemblance to that of PS II, but major differences emerge on closer examination of the phases and amplitudes. The most obvious distinction is the smaller magnitude of the Fourier transform (FT) of the PS II EXAFS compared to the FTs from the distorted cubanes. Curve fitting of the Mn EXAFS spectra verifies the known core structures of the Mn cubanes, and shows that the number of the crucial 2.7 and 3.3 Å Mn-Mn distances differs from that observed in the OEC. The EXAFS method detects small changes in the core structures as X is varied in this series, and serves to exclude the distorted cubane of C(3)(v)() symmetry as a topological model for the Mn catalytic cluster of the OEC. Instead, the method shows that even more distortion of the cubane framework, altering the ratio of the Mn-Mn distances, is required to resemble the Mn cluster in PS II.

Figure 1

Possible core structures for the active site of the OEC in PS II, containing Mn–Mn distances of 2.7–2.8 and 3.1–3.3 Å. Reprinted from ref . Copyright 1994 American Chemical Society. Only Mn and bridging O are shown.

Figure 2

Core structures of tetranuclear Mn cubane complexes: [Mn₄O₃X(OAc)₃(dbm)₃] (with X = OAc, OMe, OH, N₃, F, Cl, Br), [Mn₄O₃(OBz)(OBz)₃(dbm)₃], Mn₄O₃Cl₄(OAc)₃(py)₃ and (pyH)₃[Mn₄O₃Cl₇(OAc)₃]. Carboxylate bridges and other terminal ligands outside the cubane framework are not depicted.

Figure 3

Normalized Mn K-edge X-ray absorption near-edge structure (XANES) spectra of spinach photosystem II (PS II) preparations poised in the S₁ state and model compounds: (A) OBz, OAc, OMe, OH, N₃, and F; (B) F, Cl, Br; (C) Cl, Cl₄, and Cl₇.

Figure 4

(A) Second derivatives of the edge region of the samples in Figure 2A. (B) Second derivatives of the edge region of the samples in Figure 2B. (C) Second-derivative spectra of XANES from Figure 2C. Data were smoothed by a cubic polynomial fit over ±3.0 eV around each point.

Figure 5

Background-subtracted k-space EXAFS from PS II in the S₁ state and model compounds. For clarity, the EXAFS are Fourier-filtered using the ΔR ranges in Table 1S, and have been weighted by k . The raw k-space EXAFS spectra are available in Figure 1S. (A) OBz, OAc, OMe, OH, N₃, and F; (B) F, Cl, and Br; (C) Cl, Cl₄, and Cl₇.

Figure 6

Fourier transform spectra of raw k-space Mn EXAFS from PS II in the S₁ state and model compounds: (A) OBz, OAc, OMe, OH, N₃, and F; (B) F, Cl, and Br; (C) Cl, Cl₄, and Cl₇. The k-ranges used were the same as in Figure 4, and the minor peaks at R′ < 1 Å are due to the residual background.

Figure 7

Simulation (- - -) of Fourier transform peaks I, II, and III plotted over the Fourier-filtered k-space EXAFS (—) of OBz, OAc, OMe, and OH. Fits were generated as described in the text and Table 2 (fit labels 2, 3, 5, and 6, respectively).

Figure 8

Simulation (- - -) of Fourier transform peaks I, II, and III plotted over the Fourier-filtered k-space EXAFS (—) of N₃, F and PS II. Fits were generated as described in the text and Table 2 (fit labels 8, 9, and 15, respectively).

Figure 9

Simulation (- - -) of Fourier transform peaks I, II, and III plotted over the Fourier-filtered k-space EXAFS (—) of Cl, Br, Cl₄, and Cl₇. Fits were generated as described in the text and Table 2 (fit labels 10, 11, 12, and 14, respectively).