Thermodynamics of the S2-to-S3 state transition of the oxygen-evolving complex of photosystem II (original) (raw)
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Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II
Photosynthesis Research, 2019
The oxidation of water to O 2 is catalyzed by the Oxygen Evolving Complex (OEC), a Mn 4 CaO 5 complex in Photosystem II (PSII). The OEC is sequentially oxidized from state S 0 to S 4. The S 2 state, (Mn III)(Mn IV) 3 , coexists in two redox isomers: S 2,g=2 , where Mn4 is Mn IV and S 2,g=4.1 , where Mn1 is Mn IV. Mn4 has two terminal water ligands, whose proton affinity is affected by the Mn oxidation state. The relative energy of the two S 2 redox isomers and the protonation state of the terminal water ligands are analyzed using classical multi-conformer continuum electrostatics (MCCE). The Monte Carlo simulations are done on QM/MM optimized S 1 and S 2 structures docked back into the complete PSII, keeping the protonation state of the protein at equilibrium with the OEC redox and protonation states. Wild-type PSII, chloride-depleted PSII, PSII in the presence of oxidized Y Z /protonated D1-H190, and the PSII mutants D2-K317A, D1-D61A, and D1-S169A are studied at pH 6. The wild-type PSII at pH 8 is also described. In qualitative agreement with experiment, in wild-type PSII, the S 2,g=2 redox isomer is the lower energy state; while chloride depletion or pH 8 stabilizes the S 2,g=4.1 state and the mutants D2-K317A, D1-D61A, and D1-S169A favor the S 2,g=2 state. The protonation states of D1-E329, D1-E65, D1-H337, D1-D61, and the terminal waters on Mn4 (W1 and W2) are affected by the OEC oxidation state. The terminal W2 on Mn4 is a mixture of water and hydroxyl in the S 2,g=2 state, indicating the two water protonation states have similar energy, while it remains neutral in the S 1 and S 2,g=4.1 states. In wild-type PSII, advancement to S 2 leads to negligible proton loss and so there is an accumulation of positive charge. In the analyzed mutations and Cl − depleted PSII, additional deprotonation is found upon formation of S 2 state.
Structural changes in the S 3 state of the oxygen evolving complex in photosystem II
Chemical Physics Letters
The S 3 state of the Mn 4 CaO 5-cluster in photosystem II was investigated by DFT calculations and compared with EXAFS data. Considering previously proposed mechanism; a water molecule is inserted into an open coordination site of Mn upon S 2 to S 3 transition that becomes a substrate water, we examined if the water insertion is essential for the S 3 formation, or if one cannot eliminate other possible routes that do not require a water insertion at the S 3 stage. The novel S 3 state structure consisting of only short 2.7-2.8 Å Mn-Mn distances was discussed.
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.
Angewandte Chemie International Edition, 2013
One of the key steps in photosynthetic solar-energy conversion performed by plants, algae, and cyanobacteria is the splitting of water into molecular oxygen and hydrogen equivalents. [1] To achieve this challenging task photosynthetic organisms use a protein complex that remained almost unchanged during the evolution in the last two and a half billion years: the photosystem II (PSII). The reaction proceeds by the accumulation of four oxidizing equivalents on the {Mn 4 CaO 5 } cluster through five (S 0 -S 4 ) oxidation states that are sequentially attained during water splitting (Kok cycle). The deep understanding of the way nature has found to perform this difficult task efficiently has a great relevance not only for biology but also for inspiring the development of biomimetic artificial systems that can be used to store solar energy in an environmentally friendly way. [3] Atomic details of the structure of the oxygen-evolving complex (OEC) of PSII have been revealed by extended X-ray absorption fine structure (EXAFS) experiments and by X-ray crystallography at increasing resolution levels. [4] However, the accurate position of the {Mn 4 CaO 5 } cluster atoms and its ligands emerged only when a X-ray structure at 1.9 resolution became accessible. However, the effect of a possible X-ray photo-reduction, in particular on the characterization of the Koks state described by this structure and on the unrealistic bond lengths between the oxygen atom O5 and the two manganese ions Mn1 and Mn4, is matter of debate. Additionally, important contributions to the structure refinement came from theoretical studies. [6b, 7] Apart from a detailed characterization of the molecular structure of the OEC, an exact description of the watersplitting catalytic mechanism cannot leave aside an accurate investigation of the electronic and magnetic properties characterizing the {Mn 4 CaO 5 } cluster. In the past three decades electron paramagnetic resonance (EPR) experiments represented an extremely effective tool to explore such properties. In particular the S 2 state has been investigated in detail since the early 1980s. The S 2 EPR signals include a multiline signal (MLS) centered at g = 2.0 and a broad signal centered at g % 4.1 (reviewed by Haddy ). The MLS is indicative of a ground-state characterized by a spin S = 1/2 whereas signals at g ! 4.1 seem to be consistent with a spin S ! 5/2. Intriguingly the presence of the two signals was shown to depend on the temperature as well as on a variety of conditions in the sample preparation. In particular Casey and Sauer reported that the signal at g % 4.1 can be generated by illumination at 130 K. [8c] The subsequent warming of the sample at 200 K leads to a conversion of the signal back to the MLS. Boussac et al. [8k] showed that if the illumination is carried out on the untreated PSII in dark-adapted membranes filtering out the near-infrared component at 130 K, only the MLS is detected. Thereafter the state responsible for the MLS was converted into that corresponding to the g % 4.1 signal by excitation with near-infrared light at 150 K. Finally when temperatures of 200 K or more are reached, only the MLS is observed. Beside the large number of experiments performed on PSII in the past years, theoretical studies have provided new insights into the structural, electronic, and magnetic properties of PSII. In a recent contribution Pantazis et al. proposed the existence of two interconvertible structures consistent with the S 2 state and generating the two EPR signals. The two structures differ mainly in the position of the oxygen atom O5 (see inset in ), which is, in one case (Model A), bound to Mn4 to form a S = 1/2 spin state responsible for the MLS, and in the second case (Model B), to Mn1 in a S = 5/2 state associated with the g % 4.1 signal. The close energies and the low barriers reported for gas-phase models of the Model A and Model B, referred hereafter as S 2 A and S 2 B , suggest they can interconvert. Furthermore, it would be important for calculations to consider the effect of the full surrounding protein environment as well as the effect of molecular dynamics. Beside the importance of simulating temperature effects, the dynamic description is also crucial to escape from the local energy minima of such a complex hydrogen-bonding network. Both the temperature and environmental effects can be explicitly taken into account by ab initio molecular dynamics (AIMD) simulations performed within a quantum mechanics/ molecular mechanics framework. [6a, 13] Herein we will characterize, by AIMD using the CP2K package, [13f,g] the interconversion between the two states on different spin surfaces from the electronic, structural, and thermodynamic point of view.
Biochemistry, 2014
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.
Journal of the American Chemical Society, 2012
Extensive quantum chemical DFT calculations were performed on the high-resolution (1.9 Å) crystal structure of photosystem II in order to determine the protonation pattern and the oxidation states of the oxygenevolving Mn cluster. First, our data suggest that the experimental structure is not in the S 1 -state. Second, a rather complete set of possible protonation patterns is studied, resulting in very few alternative protonation patterns whose relevance is discussed. Finally, we show that the experimental structure is a mixture of states containing highly reduced forms, with the largest contribution (almost 60%) from the S −3 -state, Mn(II,II,III,III). 1
Chemical Communications, 2011
Synthetic access has been achieved into high oxidation state Mn/Ca chemistry with the 4 : 1 Mn : Ca stoichiometry of the oxygen-evolving complex (OEC) of plants and cyanobacteria; the anion of (Et 3 NH) 2 [Mn III 4 Ca(O 2 CPh) 4 (shi) 4 ] has a square pyramidal metal topology and an S = 0 ground state. Among the various reasons for the current intense interest in manganese chemistry is the existence of this metal at the active sites of several redox enzymes, 1 the most important of which is the oxygen-evolving complex (OEC) on the donor side of photosystem II (PS II) in green plants, algae and cyanobacteria. 2 The OEC catalyses the oxidation of H 2 O to molecular dioxygen through a four-electron process; the latter involves various oxidation states of the OEC, the so-called S n Kok states (n = 0 to 4), 3 and is the source of essentially all the O 2 on this planet. The OEC has long been known to contain four Mn and one Ca 2+ ions, 4 but the exact metal topology was only recently revealed in detail from the crystal structure of PS II from the cyanobacterium Thermosynechococcus vulcanus at 1.9 Å. 5 At this high resolution, it was seen that an oxo-bridged {Mn 3 CaO 4 } cubane-like cluster is linked to a fourth, external Mn atom via one of its bridging m 3-O 2À ions, which thus becomes m 4-, as well as via an external m 2-O 2À ion, serving to link one of the cubane Mn atoms to the external Mn atom (Scheme 1). The Mn oxidation states at the various S n Kok states involve a mixture of Mn III and Mn IV ; the dark-stable S 1 state is 2Mn III , 2Mn IV , and S 2 , the most studied Kok state, is Mn III , 3Mn IV. 6 In addition, the presence of a Ca 2+ ion is vital for the WOC activity; without its existence the OEC could not advance to the S 3 state. 7
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.
Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle
Journal of Biological Chemistry, 2013
Background: Mn 4 CaO 5 cluster catalyzes water oxidation in photosystem II. Results: Mn-Mn/Ca/ligand distances and changes in the structure of the Mn 4 CaO 5 cluster are determined for the intermediate states in the reaction using x-ray spectroscopy. Conclusion: Position of one bridging oxygen and related geometric changes may be critical during catalysis. Significance: Knowledge about structural changes during catalysis is crucial for understanding the O-O bond formation mechanism in PSII.