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Review
. 2014 Apr 23;114(8):4175-205.
doi: 10.1021/cr4004874. Epub 2014 Mar 31.

Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen

Junko Yano  1 , Vittal Yachandra
Affiliations
Review

Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen

Junko Yano et al. Chem Rev. .
No abstract available

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Figures

Figure 1
Figure 1
(a) Photosystem II structure from 1.9 Å data from X-ray crystallography showing the membrane spanning helices and the extrinsic polypeptides. The location of the cofactors involved in charge separation and the Mn4CaO5 cluster in the membrane are shown highlighted against the polypeptide background. The Mn4CaO5 cluster is on the lumenal side of the membrane with the acceptor quinones on the stromal cytoplasmic side of the membrane. (b) Cofactors on both branches of PS II shown in detail. The distances between the groups are also indicated. The figure was drawn using the coordinates from the 1.9 Å structure. Adapted from ref (27). (c) S-state Kok scheme for oxygen evolution along with proposed oxidation states of Mn in the various intermediate S-states.
Figure 2
Figure 2
Structure of the Mn4CaO5 cluster with the residues that have been identified as ligands of Mn (crimson) and Ca (green) and four water molecules (in red) from the 1.9 Å X-ray crystal structure of PS II. Oxygen is shown in yellow.
Figure 3
Figure 3
Structural models for the Mn4CaO5 cluster from (a) the polarized EXAFS and Sr EXAFS studies and (b) the 1.9 Å resolution XRD study. The Mn–Mn and Mn–O/N ligand distances from each of these studies are summarized below the respective structural model. Mn atoms are depicted in red, and Ca atoms are depicted in green. The O atoms are in gray in (a) and in yellow in (b). Reproduced with permission from ref (70). Copyright 2013 American Society for Biochemistry and Molecular Biology.
Figure 4
Figure 4
(a) Radiation damage to PS II, measured as the amount of MnII detected, is plotted as a function of incoming X-ray dose from PS II solutions (dashed lines) and crystals (solid lines). The data at two different X-ray energies (13.3 keV, where XRD experiments are conducted, and 6.6 keV) and also at two different temperatures, 100 and 10 K, are shown. The damage is mitigated by lower temperatures. The dose used for the 1.9 Å crystal structure corresponds to only ∼25% damage, whereas the dose used for the earlier crystal structures, is in excess of 70%. (b) EXAFS Fourier transforms (FTs) of PS II subjected to various degree, 5, 10, 25, and 70%, of damage compared to an FT collected with no damage (black). The decrease in intensity of the second and third FT peaks corresponds to losing the Mn–Mn and Mn–Ca distances and disruption of the bridged cluster. The first FT peak is mostly from the Mn–O bridging atoms and moves to longer distances; in the FT at 70% damage, only this one FT peak at longer distance is visible, which corresponds to that from Mn–O in the Mn(II) hexa-aquo species. (c) EXAFS FTs of PS II in S1, S0, and 25% reduced data. Figure 4a is adapted from ref (48).
Figure 5
Figure 5
Fourier transforms of the EXAFS spectra from oriented PS II crystals on the left, with the e-vector of the X-rays parallel to the a, b, and c axes of the PS II crystal lattice shown on the right. The dichroism of the FT peaks is very clear and shows the asymmetric nature of the Mn–Mn and Mn–Ca vectors. This information was used to derive three possible structural models, and one of them (model III) is shown in Figure 3a. The modified version of the structural model based on the result of the 1.9 Å crystal structure is shown in Figure 6. Adapted from ref (41).
Figure 6
Figure 6
Spectroscopic model based on data from polarized Mn EXAFS, Sr EXAFS, and EPR data, starting from the geometry of the 1.9 Å crystal structure. This structure is also similar to that proposed on the basis of DFT calculations. The major difference between this model and the 1.9 Å structure shown in Figure 3b is the asymmetric placement of the bridging O between Mn4 and Mn1, leading to an open-structure compared to a closed-structure from XRD data. Adapted from ref (80).
Figure 7
Figure 7
EXAFS data from the intermediate S-states is derived from PS II samples given 1–3 flashes. The samples do not advance completely to the next state because of misses and double hits, and hence, to obtain the pure S-state spectra, one needs to deconvolute the spectra. This is an important aspect of the spectroscopic data. This is normally accomplished by using the g = 2 multiline EPR signal from the S2 state. A typical EPR spectrum given 0–4 flashes (0F–4F) is shown in (a), with the oscillation in the intensity as a function of flashes, the best fit is shown in (b), and the calculated S-states are shown in (c). Using this matrix, one can then deconvolute the EXAFS spectra to obtain the pure S-state spectra in the S1, S2, S3, and S0 states.
Figure 8
Figure 8
(a) Fourier-transformed spectra of PS II solutions in the S0 (green), S1 (black), S2 (red), and S3 (blue) states are shown. For comparison, the spectrum of the Sn–1 state is overlaid in the S1, S2, and S3 spectra (gray). Prominent changes between the S2 and the S3 state and the S3 and the S0 state in peak II of the FT spectra are indicated by a dashed line. All spectra are shown in the same scale but with a vertical offset. (b) FTs from Mn EXAFS of the S-states from Sr-PS II. (c) FTs from Sr EXAFS show the first FT peak from Sr–O and the second FT peak from Sr–Mn. The FT peak corresponding to Sr–Mn changes during the S-state cycle and most significantly for the S2 to S3 transition. Changes are indicated by dashed lines. (a) is adapted from ref (70). (b) and (c) are adapted from ref (73).
Figure 9
Figure 9
Possible structural changes described using the spectroscopic model for the Mn4CaO5 cluster for the S1 to S2 transition. The proposed oxidation states and the main Mn–Mn distances are shown.
Figure 10
Figure 10
(a) Relation and interconvertibility of the S2-g2 and -g4 states. The S2-g2 state characterized by the multiline EPR signal can be generated from the S1 state by flash illumination at room temperature or 200 K (cw), while the S2-g4 state is generated by illumination of the S1 state at 140 K (cw)cor. The S2-g2 state can be converted to the g4 state by IR illumination at 120–140 K, and the g2 state can be produced from the g4 state by annealing at 200 K. A g4* state can be produced by treatment with F–, amines, and other treatments but cannot advance to the S3 state. (b) EPR signals from the g2 and g4 states and the g2-MLS signal generated from the g4 state by annealing at 200 K. Adapted from ref (82).
Figure 11
Figure 11
Possible structural changes described using the spectroscopic model for the Mn4CaO5 cluster for the S2 to S3 transition. The proposed oxidation states and the main Mn–Mn distances are shown. The two proposed S3 state structures are shown, where one of them is a closed structure.
Figure 12
Figure 12
Possible structural changes described using the spectroscopic model for the Mn4CaO5 cluster for the S3 to S0 transition. The proposed oxidation states and the main Mn–Mn distances are shown. The two proposed S3 and S0 state structures are shown.
Figure 13
Figure 13
Possible structural changes described using the spectroscopic model for the Mn4CaO5 cluster for the S0 to S1 transition.
Figure 14
Figure 14
Possible structural changes during the S-state transitions are illustrated. Note that the focus here is to accommodate the EXAFS distance changes, and possible protonation states (at oxo-bridging and terminal water molecules) or changes in the ligand environment (type of ligands and ligation modes) are not included in the figure. The Mn–Mn distances at ∼2.7 Å are indicated by green arrows, ∼ 2.8 Å by blue arrows and ∼3.2 Å by red arrows. The dashed line indicates that it may not be a bond. For the S3 and the S0 states, two possible models are presented. Mn atoms are shown in blue (MnIII), red (MnIV), or magenta (MnIII or MnIV possible), Ca is shown in green, and the surrounding ligand environment is shown in gray. Reproduced with permission from ref (70). Copyright 2013 American Society for Biochemistry and Molecular Biology.
Figure 15
Figure 15
First Mn EXAFS study with Ca- and Sr-substituted samples that showed that there could be a Mn–Ca/Sr interaction at ∼3.3 Å. The FT peak amplitude at ∼3.3 Å increased on Sr substitution as expected from the higher scattering cross section of Sr compared to Ca. Adapted from ref (69).
Figure 16
Figure 16
Possible structural changes described using the spectroscopic model for the Mn4CaO5 cluster for the S1 to Ca-depleted S1 state.
Figure 17
Figure 17
Ca EXAFS (left) and Sr EXAFS (right) both show scattering FT peaks from Mn in active preparations that are not present when the Mn4CaO5 cluster is disrupted using NH2OH. Both studies support a Mn–O–Ca bridging structure. Adapted from ref (46).
Figure 18
Figure 18
(a) Membranes of PS II can be oriented, and polarized EXAFS can be used to determine the orientation of Mn–Mn and Mn–Ca vectors with respect to the membrane. (b) Relative orientations of Mn–Mn and Mn–Ca vectors determined from the analysis of the data shown in (c) and (d). (c) Range-extended EXAFS of oriented membranes clearly shows the Mn–Mn vector at 3.2 Å and the Mn–Ca vector at 3.3 Å oriented differently in the PS II membrane. (d) Polarized Sr EXAFS shows the orientation of the Mn–Sr vector with respect to the membrane. Adapted from ref (46).
Figure 19
Figure 19
Summary of the Mn–Ca(Sr) distances in the S-states determined from Sr EXAFS. Adapted from ref (73).
Figure 20
Figure 20
(Top) FT of Mn EXAFS from the wild-type compared with the mutant H332E. There is a clear difference in the FTs, indicating even more asymmetry in the mutant with possible modification of a Mn–Mn distance by replacement of a His ligand by a glutamate. (Bottom) Three different structural modifications are shown as a consequence of His replacement with Glu: (a) protonation of a bridge and (b) replacement of the bidendate ligand in two different ways. One is where the Glu binds only one Mn in a bidendate manner, while in the other it is monodendate, with the possible addition of a hydroxide or water ligand. Adapted from ref (135).
Figure 21
Figure 21
Mn EXAFS spectra from monomeric and dimeric PS II. There are no differences in the Mn4CaO5 structures that are detectable from EXAFS between the dimeric and monomeric PS II.
Figure 22
Figure 22
(Left) Energy level diagram for K-emission. The dashed line (black) is the excitation into the continuum. The solid lines are the emission lines, black is 2p to 1s (Kα), red is 3p to 1s (Kβ1,3 and Kβ′), and green is valence orbitals to metal 1s (Kβ2,5 and Kβ″). The exchange interaction between the 3p and 3d makes the Kβ1,3 and the Kβ′ sensitive to the number of unpaired electrons in the 3d level and therefore the charge density (oxidation states) of Mn. The valence-to-core Kβ2,5 and Kβ″ involve the 2s and 2p levels from the ligand atoms and, hence, are sensitive to the electronic environment of the ligand. (Right) 1s2p RIXS energy level diagram. The excitation energy from 1s to 3d levels is shown as a dashed red line and is scanned using a monochromator, and the 2p-1s (Kα) emission is detected using a spherically bent crystal analyzer spectrometer. The difference between the excitation and the emission energies gives the 2p to 3d transitions, which is equivalent to the L-edges. The RIXS spectra can be used to obtain both the K-pre-edge and L-edge spectra.
Figure 23
Figure 23
(a) (Top) Mn XANES spectra from spinach PS II in all the S-states and (Bottom) the second derivatives of the Mn K-edge XANES. The inset shows the pre-edges in all the S-states. (b) (Top) Mn XANES spectra from cyanobacterial PS II in all the S-states and (Bottom) the second derivatives of the Mn K-edge XANES. The similarities in the Mn K-edge shifts in energy between spinach and cyanobacterial PS II are very clear. There are only small changes in the shape as seen in the second derivatives at around 6560 eV. The shifts in energy between the S0 to S1 and S1 to S2 are much larger than that seen for the S2 to S3 transition. This is particularly clear from the zero-crossing of the second derivatives. (c) (Top) Mn XANES spectra from spinach PS II (BBYs) and cyanobacterial PS II preparations in the dimeric form and (Bottom) the second derivatives of the Mn K-edge XANES. There are small differences in shape between the spinach and cyanobacterial PS II. These differences could arise from differences in the second sphere interactions with the Mn4Ca cluster and H-bonding network. (d) Amino acid residues within a radius of 20 Å around the Mn4Ca cluster according to the structural model of PS II from T. elongatus at 2.9 Å resolution. The right panel shows in yellow (ribbon mode) the amino acid residues within a radius of 20 Å around the Mn4Ca cluster (Mn, purple spheres; Ca, green sphere). Amino acids of subunit D1 different from spinach are highlighted in pink and are labeled in the enlarged view on the left. For better orientation, the amino acid residues Asp170, Glu189, and His332 (all of subunit D1, yellow) are labeled and are shown in stick mode. The extrinsic subunits PsbO (purple), PsbU (blue), and PsbV (light blue) are shown in cartoon mode. The view is of one monomer looking onto the monomer–monomer interface along the membrane plane (tilted by 45° to the left), with the cytoplasm above and the lumen below. (d) Adapted from ref (70).
Figure 24
Figure 24
(a) Kβ1,3 and Kβ′ spectra from MnII, MnIII, MnIV oxides. (b) 3p-3d exchange coupling that shows how the Kβ1,3 and Kβ′ spectra are sensitive to the oxidation and spin state of Mn. (c) Kβ1,3 spectra of the S-states. (d) Difference spectra which show that the shifts are larger for the S0 to S1, S1 to S2, and S3 to S0 transitions. The S2 to S3 transition is the smallest. Adapted from ref (146).
Figure 25
Figure 25
Mn K-edge inflection points from the XANES spectra (Figure 23) and the first moments from the Kβ1,3 spectra (Figure 24) shown on top and bottom, respectively. The inflection points and the first moments show that the oxidation of the OEC from the S0 to S1 and S1 to S2 is different from the S2 to S3 advance. Adapted from ref (146).
Figure 26
Figure 26
Contour plots of the 1s2p3/2 RIXS planes for four Mn oxides (A) in oxidation states II, III, and IV and the four molecular complexes (B) MnII(acac)2(H2O)2, MnIII(acac)3, [MnIII(5-Cl-Salpn)(CH3OH)2]+, and MnIV(sal)2(bipy)., The abscissa is the excitation energy, and the ordinate is the energy transfer axis. (C) Line plots extracted from the RIXS planes for the coordination complexes in oxidation states III or IV and the S1 state of PS II. The PS II plots are between oxidation states III and IV. An integration of the 2D plot parallel to the ordinate yields L-edge like spectra, the feature at ∼640 eV corresponds to transitions to J = 3/2 like states (L3 edges). Integrations parallel to the energy transfer axis sort the spectrum according to the final state. Adapted from ref (196).
Figure 27
Figure 27
(Top) K absorption pre-edges and fits for PS II in S0–S3 states (red, experimental data; black, fit; blue, pink, and green, peak components; dark gray, background). There is a lower energy peak in the fits for the S0 and S1 states, which is decreased in the S2 and S3 states. The higher-energy component increases in intensity in the S2 to S3 transition, which is consistent with the increase in Mn(IV). (Bottom) RIXS contours for PS II in S0–S3 states. The spectral changes are more subtle than those seen for the oxides and coordination complexes in Figure 26 and also compared to the multinuclear complexes in Figure 28. Adapted from ref (197).
Figure 28
Figure 28
Contour plots of Mn 1s2p RIXS planes of model compounds (a) salpn2MnIV2(OH)2, (b) salpn2MnIV2(O)(OH), (c) salpn2MnIV2(O)2, (d) phen4MnIV2(O)2, (e) MnIV3Ca2, and (f) MnIV3(O)4Acbpy.,,, The spectral features in (a), (b), and (e) with protonated bridge or with Ca are more similar to PS II S3 state spectra shown in Figure 27. Detailed theoretical analysis of spectra from model compounds such as these has the potential for understanding the electronic structure and the changes in PS II. Adapted from ref (197).
Figure 29
Figure 29
Mn Kβ1,3 and Kβ′ spectra from the high-spin and low-spin Mn(V) complexes., The exchange coupling scheme describing the two cases is shown below the spectra, which explains the lack of a Kβ′ peak in the low-spin case and the energy difference in the Kβ1,3 peak between the low- and high -pin complexes. Adapted from ref (89).
Figure 30
Figure 30
(a) Kβ′′ of the Mn in oxidation states II, III, and IV is compared to PS II in the S1 state. The position of the peak in the S1 state shows that the oxidation state is III2,IV2, and the intensity as exemplified in (b) by comparison to Mn complexes makes it clear that it is from an oxo-bridged Mn. The Mn model compounds were the following: a bridging μ-alkoxide Mn2 compound ([Mn2(II)μ-ClCH2CO2](CH3CO2)2(ClO4)2), two di-μ-oxo bridged Mn2 compounds, ([Mn2(III,IV)O2bipy4](ClO4)3 and [Mn2(IV,IV)O2terpy2(SO4)2]6(H2O)), two Mn4 cubane compounds (hexakis(μ2-diphenylphosphinato)tetrakis(μ3-oxo)Mn4(III,III,IV,IV) and [hexakis(μ2-diphenylphosphinato)tetrakis(μ3-oxo)Mn4(III,IV,IV,IV)]CF3SO3), and a macrocyclic Mn(V)-oxo complex. Adapted from ref (208).
Figure 31
Figure 31
Sensitivity of the Kβ2,5 and Kβ′′ spectra to the protonation state. This is demonstrated in the spectra of three Mn2IV oxygen-bridged complexes in which the protonation states of oxo-bridges are changed. (a) 1 and 2 show the structures of the di-μ-oxo and oxo-hydroxo bridged complexes, and 3a and 3b show the two possibilities, dihydroxo or oxo-aquo bridges. (b) Spectra of 1, 2, and 3 shown in solid black, dashed red, and dashed blue, respectively. (c) Assignments of the calculated XES valence-to-core region based on the orbital character corresponding to the individual transitions for compounds 1, 2, 3a and 3b shown in (a). The left side shows the Kβ″ region, and the right side shows the Kβ2,5 region. Adapted from ref (241).
Figure 32
Figure 32
Main mechanistic schemes that are being considered for the O–O bond formation by the Mn4CaO5 cluster.
Figure 33
Figure 33
Schematic of the simultaneous detection of X-ray diffraction and X-ray emission spectra of photosystem II crystals using the femtosecond pulses from a X-ray free electron laser (XFEL) at room temperature. The ultrashort, intense pulses from the XFEL allow one to collect data at room temperature without radiation damage, thus opening up possibilities for conducting time-resolved studies. The crystal suspension is injected using a microjet that intersects the X-ray pulses. XRD data from a single crystal are collected downstream, and XES data from the same crystal are collected at ∼90° to the beam using an XES spectrometer and a position-sensitive detector. A visible laser (527 nm) is used to illuminate the crystals to advance the PS II crystals through the S-states.
Figure 34
Figure 34
PS II structure from diffraction of micrometer-sized crystals using ∼50 fs X-ray pulses at room temperature at the XFEL. (a) Electron density map, 2mFo-DFc, for the PS II in the S1 state shown in yellow, and the electron density contoured at 1.2 σ (blue mesh) shown for a radius of 5 Å around the protein. (b) Detail of the same map in the area of the Mn4CaO5 cluster in the dark S1 state, with mesh contoured at 1.0 σ (gray) and 4.0 σ (blue). Selected residues from subunit D1 are labeled for orientation; Mn is shown as violet spheres, and Ca is shown as as an orange sphere (metal positions taken from pdb file 3bz1). (c) (Left) Kβ1,3 X-ray emission spectra from crystals (red dashed) and solutions (green) of PS II at room temperature using the XFEL. (Right) Kβ1,3 X-ray emission spectra of PS II solutions in the S1 state collected at the XFEL at room temperature (green), spectra collected using synchrotron radiation under cryogenic conditions with low dose (“8K intact”, light blue) and using synchrotron radiation at room temperature under high-dose conditions (“RT damaged”, pink). The spectrum from MnIICl2 in aqueous solution collected at room temperature is shown (gray) for comparison. The XES spectra show that the Mn4CaO5 cluster is intact in the crystals under the conditions of the XFEL experiment. Adapted from ref (62).
Figure 35
Figure 35
First data from the S1 and illuminated S2 state using the femtosecond pulses from the XFEL. This experiment shows that time-resolved crystallography of PS II at room temperature is possible. Isomorphous difference map between the XFEL-illuminated (S2 state) and the XFEL-dark (S1 state) XRD data set in the region of the Mn4CaO5 cluster, with Fo–Fo difference contours shown at +3 s (green) and −3 s (red); analysis indicates that this map is statistically featureless showing that at this resolution there are no major changes in the protein or the metal ion positions. Metal ions of the Mn4CaO5 cluster are shown for orientation as violet (Mn) and orange (Ca) spheres; subunits are indicated in yellow (D1), orange (D2), pink (CP43), and green (PsbO). Adapted from ref (62).
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