Toward understanding the S2-S3 transition in the Kok cycle of Photosystem II: Lessons from Sr-substituted structure (original) (raw)
Related papers
Energy & Environmental Science, 2012
The water-splitting protein, photosystem II, catalyzes the light-driven oxidation of water to dioxygen. The solar water oxidation reaction takes place at the catalytic center, referred to as the oxygen-evolving complex, of photosystem II. During the catalytic cycle, the oxygen-evolving complex cycles through five distinct intermediate states, S 0 -S 4 . In this study, we trap the oxygen-evolving complex in the S 2 intermediate state by low temperature illumination of photosystem II isolated from three different species, Thermosynechococcus vulcanus, the PsbB variant of Synechocystis PCC 6803 and spinach. We apply two-dimensional hyperfine sublevel correlation spectroscopy to detect weak magnetic interactions between the paramagnetic tetra-nuclear manganese cluster of the S 2 state of the OEC and the surrounding protons. We identify five groups of protons that are interacting with the tetra-nuclear manganese cluster. From the values of hyperfine interactions and using the recently reported 1.9
Assignment of the μ4-O5 atom in catalytic center for water oxidation in photosystem II
Chinese Science Bulletin, 2013
The detailed structure of catalytic center of water oxidation, Mn 4 Ca-cluster, in photosystem II (PSII) has been reported recently. However, due to the radiation damage induced by X-ray and the complexity of the Mn 4 Ca-cluster, the assignment of the 4-O5 atom coordinated by three Mn and one Ca 2+ ions is still lack of essential evidences. In this article, we synthesized one Mn complex containing two 4-O atoms. It is found that the lengths of all 4-O-Mn bonds in this Mn complex are in the range of 1.89-2.10 Å, which are significantly shorter than 2.40-2.61 Å distance of 4-O5-Mn bonds in Mn 4 Ca-cluster observed in the crystal structure of PSII. In addition, DFT calculations have been carried out on the Mn 4 Ca-cluster. It is found that the O atom of 4-O or 4-OH always trends to deviate from the center position of four metal ions, resulting in unequal bond lengths of four 4-O-M (M=Mn or Ca), which is obviously different with larger and nearly equal distances between 4-O and four metal ions observed in the crystal structure. Based on these results, we suggest that the 4-atom in Mn 4 Ca-cluster of PSII is unlikely to be a 4-O, 4-OH or 4-OH 2 , and its assignment is still an open question.
Proceedings of the National Academy of Sciences
In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2 → S3 transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O2 formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2 → S3 transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QA and QB, are observed. At the donor site, tyrosine YZ and His190 H-bonded to it move by 50 µs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of OX(H) at the open coordination site o...
Journal of The American Chemical Society, 2008
This paper investigates the mechanism of water splitting in photosystem II (PSII) as described by chemically sensible models of the oxygen-evolving complex (OEC) in the S0-S4 states. The reaction is the paradigm for engineering direct solar fuel production systems since it is driven by solar light and the catalyst involves inexpensive and abundant metals (calcium and manganese). Molecular models of the OEC Mn 3CaO4Mn catalytic cluster are constructed by explicitly considering the perturbational influence of the surrounding protein environment according to state-of-the-art quantum mechanics/molecular mechanics (QM/MM) hybrid methods, in conjunction with the X-ray diffraction (XRD) structure of PSII from the cyanobacterium Thermosynechococcus elongatus. The resulting models are validated through direct comparisons with high-resolution extended X-ray absorption fine structure spectroscopic data. Structures of the S3, S4, and S0 states include an additional µ-oxo bridge between Mn(3) and Mn , not present in XRD structures, found to be essential for the deprotonation of substrate water molecules. The structures of reaction intermediates suggest a detailed mechanism of dioxygen evolution based on changes in oxidization and protonation states and structural rearrangements of the oxomanganese cluster and surrounding water molecules. The catalytic reaction is consistent with substrate water molecules coordinated as terminal ligands to Mn(4) and calcium and requires the formation of an oxyl radical by deprotonation of the substrate water molecule ligated to Mn(4) and the accumulation of four oxidizing equivalents. The oxyl radical is susceptible to nucleophilic attack by a substrate water molecule initially coordinated to calcium and activated by two basic species, including CP43-R357 and the µ-oxo bridge between Mn(3) and Mn(4). The reaction is concerted with water ligand exchange, swapping the activated water by a water molecule in the second coordination shell of calcium. † Current address:
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.
Pathway for Mn-cluster oxidation by tyrosine-Z in the S2 state of photosystem II
Proceedings of the National Academy of Sciences
Water oxidation in photosynthetic organisms occurs through the five intermediate steps S 0 -S 4 of the Kok cycle in the oxygen evolving complex of photosystem II (PSII). Along the catalytic cycle, four electrons are subsequently removed from the Mn 4 CaO 5 core by the nearby tyrosine Tyr-Z, which is in turn oxidized by the chlorophyll special pair P680, the photo-induced primary donor in PSII. Recently, two Mn 4 CaO 5 conformations, consistent with the S 2 state (namely, S A 2 and S B 2 models) were suggested to exist, perhaps playing a different role within the S 2 -to-S 3 transition. Here we report multiscale ab initio density functional theory plus U simulations revealing that upon such oxidation the relative thermodynamic stability of the two previously proposed geometries is reversed, the S B 2 state becoming the leading conformation. In this latter state a proton coupled electron transfer is spontaneously observed at ∼100 fs at room temperature dynamics. Upon oxidation, the Mn cluster, which is tightly electronically coupled along dynamics to the Tyr-Z tyrosyl group, releases a proton from the nearby W1 water molecule to the close Asp-61 on the femtosecond timescale, thus undergoing a conformational transition increasing the available space for the subsequent coordination of an additional water molecule. The results can help to rationalize previous spectroscopic experiments and confirm, for the first time to our knowledge, that the water-splitting reaction has to proceed through the S B 2 conformation, providing the basis for a structural model of the S 3 state.
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.
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.