Simulation of S₂-State Multiline EPR Signal in Oriented Photosystem II Membranes:  Structural Implications for the Manganese Cluster in an Oxygen-Evolving Complex

Abstract

High-quality angular-dependent spectra of multiline electron paramagnetic resonance (EPR) signals from the S2-state Mn cluster in a photosynthetic oxygen-evolving complex (OEC) were obtained for partially oriented photosystem (PS) II membranes, and the magnetic structure of the Mn cluster has been studied by simulation analysis. The angular-dependent multiline spectra were simulated by taking into account the anisotropic properties of both hyperfine tensors of intrinsic Mn ions and g-tensor of the cluster in a tetranuclear model. The best-fit parameters for the simulation indicate that (a) the oxidation state of the S2-state Mn cluster is Mn(III, IV, IV, IV), (b) the electronic orbital configuration of the Mn(III) ion is (dpi)3[dz2(sigma))]1, (c) the effective g-tensor of the Mn cluster and the hyperfine tensor of the Mn(III) ion are axially symmetric, and their principal z-axes are nearly collinear each other, and (d) the z-axis of the dz2 orbital of the Mn(III) ion and the normal of the thylakoid membrane are at an angle of 50.1 +/- 1.8 degrees. The results are compatible with those of the oriented XAFS study [Mukerji, I., et al. (1994) Biochemistry 33, 9712-9721], and indicate that the O-O vector of the putative di-mu-oxo bridged Mn(III)-Mn(IV) dimer unit in the Mn cluster tilts by 43-56 degrees with respect to the normal of thylakoid membrane. A model of the arrangement of the di-mu-oxo bridged Mn(III)-Mn(IV) unit with respect to the thylakoid membrane is proposed.

Absence of Mn-Centered Oxidation in the S2 → S3 Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

“…In addition, simulations of the EPR signals from the S 2 state also provide insight into the absolute Mn oxidation states in the S 2 state. S 2 -state EPR multiline signal simulations by Hasegawa et al 96,97 and 55 Mn ENDOR spectroscopy on the S 2 state by Britt and co-workers 98,99 100,101 the 2nd derivative of the XANES spectrum for the S 1 state shows that its edge shape is unlike the edge shape observed for Mn(III) complexes; when the 2nd-derivative XANES spectrum for the S 1 state is fit using Mn(III) and Mn(IV) model compounds, it cannot be fit well using only Mn(III) model compounds. 18,102 Furthermore, inspection of the only available set of tetranuclear Mn complexes with all O ligation, four distorted Mn 4 (III 3 ,IV) cubanes, shows XANES IPE values at ~6551 eV for these complexes, 20 consistent with the S 0 -state XANES IPE of 6550.8 eV and lower than the S 1 -state XANES IPE of 6552.9 eV.…”

Photosystem II and photosynthetic oxidation of water: an overview

“…three tightly coupled and one weakly coupled Mn) were discussed. Recently, they have received renewed attention (Hasegawa et al 1998;Peloquin & Britt 2001), especially with the benefit of the recent crystallographic model (Carrell et al 2001) (see Zouni et al 2001; figure 3). …”

XANES, EXAFS and Kbeta spectroscopic studies of the oxygen-evolving complex in Photosystem II

“…52,53 In addition, the S 1 state has a parallel-polarization EPR signal. [47][48][49]84 These signals have been interpreted as arising from a Mn cluster with a nuclearity of four, 75,76,142,190 although other interpretations exist. 191,192 Two forms of X-ray spectroscopy, X-ray aborption near-edge structure (XANES) spectroscopy and extended X -ray absorption fine structure (EXAFS) spectroscopy, have provided a wealth of information about the oxidation states of Mn in the OEC and the structure of the OEC, respectively, in the S 1 and S 2 states.…”

“…60 The current data lack sufficient resolution to define an exact structure of the OEC in the S 1 state, but suggest an asymmetric 'Y' shape of the cluster. Based on 55 Mn ENDOR data from the S 2 -state multiline EPR signal, 44,74 continuous-wave EPR simulations of the S 2 -state EPR multiline signal, 75,76 and density functional theory (DFT) calculations, 77 structural models with a monomer-trimer arrangement of the Mn ions have been proposed, while a recent simulation of the S 2 -state multiline EPR signal is consistent with a diamond-like structure. 78 Further work is required to define the overall structure of the OEC, but the Mn-Mn and Mn-Ca vectors determined by EXAFS spectroscopy will serve as a basis for any proposed structure.…”