Oxygen-Evolving Mn Cluster in Photosystem II: The Protonation Pattern and Oxidation State in the High-Resolution Crystal Structure (original) (raw)
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Electronic Structure and Oxidation State Changes in the Mn4Ca Cluster of Photosystem II
Photosynthesis. Energy from the Sun, 2008
Oxygen-evolving complex (Mn 4 Ca cluster) of Photosystem II cycles through five intermediate states (S i-states, i =0-4) before a molecule of dioxygen is released. During the S-state transitions, electrons are extracted from the OEC, either from Mn or alternatively from a Mn ligand. The oxidation state of Mn is widely accepted as Mn 4 (III 2 ,IV 2) and Mn 4 (III,IV 3) for S 1 and S 2 states, while it is still controversial for the S 0 and S 3 states. We used resonant inelastic X-ray scattering (RIXS) to study the electronic structure of Mn 4 Ca complex in the OEC. The RIXS data yield twodimensional plots that provide a significant advantage by obtaining both K-edge pre-edge and Ledge like spectra (metal spin state) simultaneously. We have collected data from PSII samples in the each of the S-states and compared them with data from various inorganic Mn complexes. The spectral changes in the Mn 1s2p 3/2 RIXS spectra between the S-states were compared to those of the oxides of Mn and coordination complexes. The results indicate strong covalency for the electronic configuration in the OEC, and we conclude that the electron is transferred from a strongly delocalized orbital, compared to those in Mn oxides or coordination complexes. The magnitude for the S 0 to S 1 , and S 1 to S 2 transitions is twice as large as that during the S 2 to S 3 transition, indicating that the electron for this transition is extracted from a highly delocalized orbital with little change in charge density at the Mn atoms.
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.
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.
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, 2005
Figure 1. Left: A schematic representation of the detection scheme. Mn and Fe Kα1 and Kα2 fluorescence peaks are ~5eV wide and split by ~11eV (not shown). The multi-crystal monochromator with ~1 eV resolution is tuned to the Kα1 peak (red). The fluorescence peaks broadened by the Ge-detector with 150-200eV resolution are shown below (blue). 17 Right: The PS II Mn K-edge EXAFS spectrum from the S 1 state sample obtained with a traditional energy-discriminating Ge-detector (blue) compared, with that collected using the highresolution crystal monochromator (red). Fe present in PS II does not pose a problem with the high-resolution detector (the Fe edge is marked by a green line). Inset: The inset shows the schematic for the crystal monochromator used in a backscattering configuration. 12
Biophysical Journal, 2010
The solar water-splitting protein complex, photosystem II, catalyzes the light-driven oxidation of water to dioxygen in Nature. The four-electron oxidation reaction of water occurs at the tetranuclear manganese-calcium-oxo catalytic cluster that is present in the oxygen-evolving complex of photosystem II. The mechanism of light-driven water oxidation has been a subject of intense interest, and the oxygenevolving complex of photosystem II has been studied extensively by structural and biochemical methods. While the recent X-ray crystal structures and single-crystal EXAFS investigations provide a model for the geometry of the tetranuclear manganese-calcium-oxo catalytic cluster, there is limited knowledge of the protein environment that surrounds the catalytic cluster. In this study, we demonstrate the application of two-dimensional hyperfine sublevel correlation spectroscopy to determine the magnetic couplings of the catalytic cluster with the 14 N atoms of surrounding amino acid residues in the S 2 state of the oxygen-evolving complex of photosystem II. We utilize two-dimensional difference spectroscopy to facilitate unambiguous assignments of the spectral features and identify at least three separate 14 N atoms that are interacting with the catalytic cluster in the S 2 state. The results presented here, for the first time, identify previously unknown ligands to the catalytic cluster of photosystem II and provide avenues for the assignment of residues by site-directed mutagenesis and the refinement of computational and mechanistic models of photosystem II.
Physical Chemistry Chemical Physics, 2005
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 (B2.7 Å and B3.3 Å ) that have been observed in the OEC. Model complexes with core compositions Mn 3 O and Mn 4 O 2 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 Kb 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...
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.
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.