An e.x.a.f.s. study of the manganese O2-evolving complex in purified Photosystem II membrane fractions. The S1 and S2 states.
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ABSTRACT:
SUBMITTER: MacLachlan DJ
PROVIDER: S-EPMC1132826 | biostudies-other | 1992 Jul
REPOSITORIES: biostudies-other
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Project description:We introduce a quantum mechanics/molecular mechanics model of the oxygen-evolving complex of photosystem II in the S(1) Mn(4)(IV,III,IV,III) state, where Ca(2+) is bridged to manganese centers by the carboxylate moieties of D170 and A344 on the basis of the new X-ray diffraction (XRD) model recently reported at 1.9 Å resolution. The model is also consistent with high-resolution spectroscopic data, including polarized extended X-ray absorption fine structure data of oriented single crystals. Our results provide refined intermetallic distances within the Mn cluster and suggest that the XRD model most likely corresponds to a mixture of oxidation states, including species more reduced than those observed in the catalytic cycle of water splitting.
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Project description:Mechanistic investigations of the water-splitting reaction of the oxygen-evolving complex (OEC) of photosystem II (PSII) are fundamentally informed by structural studies. Many physical techniques have provided important insights into the OEC structure and function, including X-ray diffraction (XRD) and extended X-ray absorption fine structure (EXAFS) spectroscopy as well as mass spectrometry (MS), electron paramagnetic resonance (EPR) spectroscopy, and Fourier transform infrared spectroscopy applied in conjunction with mutagenesis studies. However, experimental studies have yet to yield consensus as to the exact configuration of the catalytic metal cluster and its ligation scheme. Computational modeling studies, including density functional (DFT) theory combined with quantum mechanics/molecular mechanics (QM/MM) hybrid methods for explicitly including the influence of the surrounding protein, have proposed chemically satisfactory models of the fully ligated OEC within PSII that are maximally consistent with experimental results. The inorganic core of these models is similar to the crystallographic model upon which they were based, but comprises important modifications due to structural refinement, hydration, and proteinaceous ligation which improve agreement with a wide range of experimental data. The computational models are useful for rationalizing spectroscopic and crystallographic results and for building a complete structure-based mechanism of water-splitting in PSII as described by the intermediate oxidation states of the OEC. This review summarizes these recent advances in QM/MM modeling of PSII within the context of recent experimental studies.
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Project description:The S1 ? S2 transition of the oxygen-evolving complex (OEC) of photosystem II does not involve the transfer of a proton to the lumen and occurs at cryogenic temperatures. Therefore, it is commonly thought to involve only Mn oxidation without any significant change in the structure of the OEC. Here, we analyze structural changes upon the S1 ? S2 transition, as revealed by quantum mechanics/molecular mechanics methods and the isomorphous difference Fourier method applied to serial femtosecond X-ray diffraction data. We find that the main structural change in the OEC is in the position of the dangling Mn and its coordination environment.
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Project description: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.
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Project description:The oxygen-evolving complex of Photosystem II (PS II) in green plants and algae contains a cluster of four manganese atoms in the active site, which catalyzes the photoinduced oxidation of water to dioxygen. Along with Mn, calcium and chloride ions are necessary cofactors for proper functioning of the complex. A key unresolved question is whether Ca is close to the Mn cluster, within about 3.5 Å. To further test and verify this finding, we substituted strontium for Ca and probed from the Sr point-of-view for any nearby Mn. Sr has been shown to replace Ca and still maintain enzyme activity (about 40% of normal rate). The extended X-ray absorption fine structure (EXAFS) of Sr-PS II probes the local environment around the Sr cofactor to detect any nearby Mn. We focused on the functional Sr by removing nonessential, loosely bound Sr in the protein environment. For comparison, an inactive sample was prepared by treating the intact PS II with hydroxylamine to disrupt the Mn cluster and to produce nonfunctional enzyme. Sr EXAFS results indicate major differences in the phase and amplitude between the functional (intact) and nonfunctional (NH2OH-treated) samples. In intact samples, the Fourier transform of the Sr EXAFS shows a peak that is missing in inactive samples. This Fourier peak II is best simulated by two Mn neighbors at a distance of 3.5 Å. Thus, with X-ray absorption studies on Sr-reconstituted PS II, we confirm the proximity of Ca (Sr) cofactor to the Mn cluster and show that the active site is a Mn-Ca heteronuclear cluster.
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Project description:Robust oxygenic photosynthesis requires a suite of accessory factors to ensure efficient assembly and repair of the oxygen-evolving photosystem two (PSII) complex. The highly conserved Ycf48 assembly factor binds to the newly synthesized D1 reaction center polypeptide and promotes the initial steps of PSII assembly, but its binding site is unclear. Here we use cryo-electron microscopy to determine the structure of a cyanobacterial PSII D1/D2 reaction center assembly complex with Ycf48 attached. Ycf48, a 7-bladed beta propeller, binds to the amino-acid residues of D1 that ultimately ligate the water-oxidising Mn4CaO5 cluster, thereby preventing the premature binding of Mn2+ and Ca2+ ions and protecting the site from damage. Interactions with D2 help explain how Ycf48 promotes assembly of the D1/D2 complex. Overall, our work provides valuable insights into the early stages of PSII assembly and the structural changes that create the binding site for the Mn4CaO5 cluster.
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Project description:The S2 state produces two basic electron paramagnetic resonance signal types due to the manganese cluster in oxygen-evolving complex, which are influenced by the solvents, and cryoprotectant added to the photosystem II samples. It is presumed that a single manganese center oxidation occurs on S1 → S2 state transition. The S2 state has readily visible multiline and g4.1 electron paramagnetic resonance signals and hence it has been the most studied of all the Kok cycle intermediates due to the ease of experimental preparation and stability. The S2 state was studied using electron paramagnetic resonance spectroscopy at X-band frequencies. The aim of this study was to determine the spin states of the g4.1 signal. The multiline signal was observed to arise from a ground state spin ½ centre while the g4.1 signal generated at ≈140 K NIR illumination was proposed to arise from a spin 52 center with rhombic distortion. The 'ground' state g4.1 signal was generated solely or by conversion from the multiline. The data analysis methods used involved numerical simulations of the experimental spectra on relevant models of the oxygen-evolving complex cluster. A strong focus in this paper was on the 'ground' state g4.1 signal, whether it is a rhombic 52 spin state signal or an axial 32 spin state signal. The data supported an X-band CW-EPR-generated g4.1 signal as originating from a near rhombic spin 5/2 of the S2 state of the PSII manganese cluster.
| S-EPMC8125536 | biostudies-literature
Project description:Most of the main features of water oxidation in photosystem II are now well understood, including the mechanism for O-O bond formation. For the intermediate S2 and S3 structures there is also nearly complete agreement between quantum chemical modeling and experiments. Given the present high degree of consensus for these structures, it is of high interest to go back to previous suggestions concerning what happens in the S2-S3 transition. Analyses of extended X-ray adsorption fine structure (EXAFS) experiments have indicated relatively large structural changes in this transition, with changes of distances sometimes larger than 0.3 Å and a change of topology. In contrast, our previous density functional theory (DFT)(B3LYP) calculations on a cluster model showed very small changes, less than 0.1 Å. It is here found that the DFT structures are also consistent with the EXAFS spectra for the S2 and S3 states within normal errors of DFT. The analysis suggests that there are severe problems in interpreting EXAFS spectra for these complicated systems.
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Project description:In biological water oxidation, a redox-active tyrosine residue (D1-Tyr161 or YZ) mediates electron transfer between the Mn4CaO5 cluster of the oxygen-evolving complex and the charge-separation site of photosystem II (PSII), driving the cluster through progressively higher oxidation states S i ( i = 0-4). In contrast to lower S-states (S0, S1), in higher S-states (S2, S3) of the Mn4CaO5 cluster, YZ cannot be oxidized at cryogenic temperatures due to the accumulation of positive charge in the S1 → S2 transition. However, oxidation of YZ by illumination of S2 at 77-190 K followed by rapid freezing and charge recombination between YZ• and the plastoquinone radical QA•- allows trapping of an S2 variant, the so-called S2trapped state (S2t), that is capable of forming YZ• at cryogenic temperature. To identify the differences between the S2 and S2t states, we used the S2tYZ• intermediate as a probe for the S2t state and followed the S2tYZ•/QA•- recombination kinetics at 10 K using time-resolved electron paramagnetic resonance spectroscopy in H2O and D2O. The results show that while S2tYZ•/QA•- recombination can be described as pure electron transfer occurring in the Marcus inverted region, the S2t → S2 reversion depends on proton rearrangement and exhibits a strong kinetic isotope effect. This suggests that YZ oxidation in the S2t state is facilitated by favorable proton redistribution in the vicinity of YZ, most likely within the hydrogen-bonded YZ-His190-Asn298 triad. Computational models show that tautomerization of Asn298 to its imidic acid form enables proton translocation to an adjacent asparagine-rich cavity of water molecules that functions as a proton reservoir and can further participate in proton egress to the lumen.
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Project description:In the recent X-ray crystallographic structural models of photosystem II, Glu189 of the D1 polypeptide is assigned as a ligand of the oxygen-evolving Mn(4) cluster. To determine if D1-Glu189 ligates a Mn ion that undergoes oxidation during one or more of the S(0) --> S(1), S(1) --> S(2), and S(2) --> S(3) transitions, the FTIR difference spectra of the individual S-state transitions in D1-E189Q and D1-E189R mutant PSII particles from the cyanobacterium Synechocystis sp. PCC 6803 were compared with those in wild-type PSII particles. Remarkably, the data show that neither mutation significantly alters the mid-frequency regions (1800-1200 cm(-)(1)) of any of the FTIR difference spectra. Importantly, neither mutation eliminates any specific symmetric or asymmetric carboxylate stretching mode that might have been assigned to D1-Glu189. The small spectral alterations that are observed are similar in amplitude to those that are observed in wild-type PSII particles that have been exchanged into FTIR analysis buffer by different methods or those that are observed in D2-H189Q mutant PSII particles (the residue D2-His189 is located >25 A from the Mn(4) cluster and accepts a hydrogen bond from Tyr Y(D)). The absence of significant mutation-induced spectral alterations in the D1-Glu189 mutants shows that the oxidation of the Mn(4) cluster does not alter the frequencies of the carboxylate stretching modes of D1-Glu189 during the S(0) --> S(1), S(1) --> S(2), or S(2) --> S(3) transitions. One explanation of these data is that D1-Glu189 ligates a Mn ion that does not increase its charge or oxidation state during any of these S-state transitions. However, because the same conclusion was reached previously for D1-Asp170, and because the recent X-ray crystallographic structural models assign D1-Asp170 and D1-Glu189 as ligating different Mn ions, this explanation requires that (1) the extra positive charge that develops on the Mn(4) cluster during the S(1) --> S(2) transition be localized on the Mn ion that is ligated by the alpha-COO(-) group of D1-Ala344 and (2) any increase in positive charge that develops on the Mn(4) cluster during the S(0) --> S(1) and S(2) --> S(3) transitions be localized on the one Mn ion that is not ligated by D1-Asp170, D1-Glu189, or D1-Ala344. An alternative explanation of the FTIR data is that D1-Glu189 does not ligate the Mn(4) cluster. This conclusion would be consistent with earlier spectroscopic analyses of D1-Glu189 mutants, but would require that the proximity of D1-Glu189 to manganese in the X-ray crystallographic structural models be an artifact of the radiation-induced reduction of the Mn(4) cluster that occurred during the collection of the X-ray diffraction data.
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