Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to photosystem II: Mn Kedge x-ray absorption and K-Beta X-ray emission spectroscopy studies (original) (raw)
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Physical Chemistry Chemical Physics, 2004
X-Ray spectroscopy is used to examine the effect of the manganese oxidation state for a series of Mn model compounds. Sensitive to Mn oxidation and structural symmetry, X-ray absorption and emission spectroscopy (XAS and XES) provide complementary insights. However, few benchmark examples of complexes with similar structures but in different oxidation states are available to evaluate data from unknown structures like the oxygen evolving complex (OEC) of Photosystem II (PSII). This study examines two types of compounds prepared in a variety of Mn oxidation states and which possess chemical structures with Mn-Mn interactions (~2.7 Å and ~3.3 Å) that have been observed in the OEC. Model complexes with core compositions Mn3O and Mn4O2 contain combinations of Mn in either a reduced (II) or oxidized (III) state. Within each set of compounds, complexes with higher Mn oxidation states have absorption K-edge energy values that are higher (1.6-2.2 eV) than those of their more reduced counterparts. This trend is accordingly reversed in the Kβ emission spectroscopy where the first moment energy values are lower (0.09-0.12 eV) for compounds with higher Mn oxidation states. We will discuss in detail, how these trends can be quantitatively used to characterize the effects of the Mn oxidation state as well as the surrounding ligand environment on the observed X-ray spectra. The results are discussed with respect to previously obtained data on different S-states of the OEC.
Physical chemistry chemical physics : PCCP, 2004
X-Ray spectroscopy is used to examine the effect of the manganese oxidation state for a series of Mn model compounds. Sensitive to Mn oxidation and structural symmetry, X-ray absorption and emission spectroscopy (XAS and XES) provide complementary insights. However, few benchmark examples of complexes with similar structures but in different oxidation states are available to evaluate data from unknown structures like the oxygen evolving complex (OEC) of Photosystem II (PSII). This study examines two types of compounds prepared in a variety of Mn oxidation states and which possess chemical structures with Mn-Mn interactions (~2.7 Å and ~3.3 Å) that have been observed in the OEC. Model complexes with core compositions Mn3O and Mn4O2 contain combinations of Mn in either a reduced (II) or oxidized (III) state. Within each set of compounds, complexes with higher Mn oxidation states have absorption K-edge energy values that are higher (1.6-2.2 eV) than those of their more reduced counterp...
Characterization of the Mn Oxidation States in Photosystem II by Kβ X-ray Fluorescence Spectroscopy
The Journal of Physical Chemistry B, 1998
The nature of the Mn oxidation states involved in photosynthetic oxygen evolution has remained controversial, despite intense study by X-ray absorption and electron paramagnetic resonance spectroscopy. As an alternative approach, high-resolution K X-ray fluorescence spectra have been recorded on the dark-adapted S 1 state and the hydroquinone-reduced state of the oxygen-evolving complex in photosystem II. By comparison of the K chemical shifts with those of appropriate model compounds, the S 1 state of photosystem II is found to contain equal amounts of Mn(III) and Mn(IV). In the hydroquinone-reduced sample, a significant fraction of the Mn is reduced to Mn(II). The results are compatible with models involving conversion of Mn(III) 2 Mn-(IV) 2 to Mn(II) 2 Mn(IV) 2 clusters.
Journal of the American Chemical Society, 2007
High-valent Mn-oxo species have been suggested to have a catalytically important role in the water splitting reaction which occurs in the Photosystem II membrane protein. In this study, five-and sixcoordinate mononuclear Mn(V) compounds were investigated by polarized X-ray absorption spectroscopy in order to understand the electronic structure and spectroscopic characteristics of high-valent Mn species. Single crystals of the Mn(V)-nitrido and Mn(V)-oxo compounds were aligned along selected molecular vectors with respect to the X-ray polarization vector using X-ray diffraction. The local electronic structure of the metal site was then studied by measuring the polarization dependence of X-ray absorption near-edge spectroscopy (XANES) pre-edge spectra (1s to 3d transition) and comparing with the results of density functional theory (DFT) calculations. The Mn(V)-nitrido compound, in which the manganese is coordinated in a tetragonally distorted octahedral environment, showed a single dominant pre-edge peak along the MntN axis that can be assigned to a strong 3d z 2-4pz mixing mechanism. In the square pyramidal Mn-(V)-oxo system, on the other hand, an additional peak was observed at 1 eV below the main pre-edge peak. This component was interpreted as a 1s to 3dxz,yz transition with 4px,y mixing, due to the displacement of the Mn atom out of the equatorial plane. The XANES results have been correlated to DFT calculations, and the spectra have been simulated using a TD (time-dependent)-DFT approach. The relevance of these results to understanding the mechanism of the photosynthetic water oxidation is discussed.
Journal of the American Chemical Society, 2004
Resonant inelastic X-ray scattering (RIXS) was used to collect Mn K pre-edge spectra and to study the electronic structure in oxides, molecular coordination complexes, as well as the S1 and S2 states of the oxygen-evolving complex (OEC) of photosystem II (PS II). The RIXS data yield two-dimensional plots that can be interpreted along the incident (absorption) energy or the energy transfer axis. The second energy dimension separates the pre-edge (predominantly 1s to 3d transitions) from the main K-edge, and a detailed analysis is thus possible. The 1s2p RIXS final-state electron configuration along the energy transfer axis is identical to conventional Ledge absorption spectroscopy, and the RIXS spectra are therefore sensitive to the Mn spin state. This new technique thus yields information on the electronic structure that is not accessible in conventional K-edge absorption spectroscopy. The line splittings can be understood within a ligand field multiplet model, i.e., (3d,3d) and (2p,3d) two-electron interactions are crucial to describe the spectral shapes in all systems. We propose to explain the shift of the K pre-edge absorption energy upon Mn oxidation in terms of the effective number of 3d electrons (fractional 3d orbital population). The spectral changes in the Mn 1s2p 3/2 RIXS spectra between the PS II S1 and S2 states are small compared to that of the oxides and two of the coordination complexes (Mn III (acac)3 and Mn IV (sal)2(bipy)). We conclude that the electron in the step from S1 to S2 is transferred from a strongly delocalized orbital.
Inorganic Chemistry, 2013
The oxygen-evolving complex (OEC) in photosystem II (PS II) was studied in the S 0 through S 3 states using 1s2p resonant inelastic X-ray scattering spectroscopy. The spectral changes of the OEC during the S-state transitions are subtle, indicating that the electrons are strongly delocalized throughout the cluster. The result suggests that, in addition to the Mn ions, ligands are also playing an important role in the redox reactions. A series of Mn IV coordination complexes were compared, particularly with the PS II S 3 state spectrum to understand its oxidation state. We find strong variations of the electronic structure within the series of Mn IV model systems. The spectrum of the S 3 state best resembles those of the Mn IV complexes Mn 3 IV Ca 2 and saplnMn 2 IV (OH) 2. The current result emphasizes that the assignment of formal oxidation states alone is not sufficient for understanding the detailed electronic structural changes that govern the catalytic reaction in the OEC.
Biophysical Journal, 2003
In oxygenic photosynthesis, water is oxidized at a protein-cofactor complex comprising four Mn atoms and, presumably, one calcium. Using multilayers of Photosystem II membrane particles, we investigated the time course of the disassembly of the Mn complex initiated by a temperature jump from 258C to 478C and terminated by rapid cooling after distinct heating periods. We monitored polarographically the oxygen-evolution activity, the amount of the Y D ox radical and of released Mn 2þ by EPR spectroscopy, and the structure of the Mn complex by x-ray absorption spectroscopy (XAS, EXAFS). Using a novel approach to analyze time-resolved EXAFS data, we identify three distinct phases of the disassembly process: (1) Loss of the oxygen-evolution activity and reduction of Y D ox occur simultaneously (k 1 ¼ 1.0 min ÿ1). EXAFS spectra reveal the concomitant loss of an absorber-backscatterer interaction between heavy atoms separated by ;3.3 Å , possibly related to Ca release. (2) Subsequently, two Mn(III) or Mn(IV) ions seemingly separated by ;2.7 Å in the native complex are reduced to Mn(II) and released (k 2 ¼ 0.18 min ÿ1). The x-ray absorption spectroscopy data is highly suggestive that the two unreleased Mn ions form a dim -oxo bridged Mn(III) 2 complex. (3) Finally, the tightly-bound Mn 2 (m-O) 2 unit is slowly reduced and released (k 3 ¼ 0.014 min ÿ1).
Biochemistry, 1990
Hydroxylamine at low concentrations causes a two-flash delay in the first maximum flash yield of oxygen evolved from spinach photosystem II (PSII) subchloroplast membranes that have been excited by a series of saturating flashes of light. Untreated PSII membrane preparations exhibit a multiline EPR signal assigned to a manganese cluster and associated with the S2 state when illuminated at 195 K, or at 273 K in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU). We used the extent of suppression of the multiline EPR signal observed in samples illuminated at 195 K to determine the fraction of PSII reaction centers set back to a hydroxylamine-induced S0-like state, which we designate S0*. The manganese K-edge X-ray absorption edges for dark-adapted PSII preparations with or without hydroxylamine are virtually identical. This indicates that, despite its high binding affinity to the oxygen-evolving complex (OEC) in the dark, hydroxylamine does not reduce chemically the manganese cluster within the OEC in the dark. After a single turnover of PSII, a shift to lower energy is observed in the inflection of the Mn K-edge of the manganese cluster. We conclude that, in the presence of hydroxylamine, illumination causes a reduction of the OEC, resulting in a state resembling S0. This lower Mn K-edge energy of S0*, relative to the edge of S1, implies the storage and stabilization of an oxidative equivalent within the manganese cluster during the S0----S1 state transition. An analysis of the extended X-ray absorption fine structure (EXAFS) of the S0* state indicates that a significant structural rearrangement occurs between the S0* and S1 states. The X-ray absorption edge position and the structure of the manganese cluster in the S0* state are indicative of a heterogeneous mixture of formal valences of manganese including one Mn(II) which is not present in the S1 state.