Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen‐Evolving Complex of Photosystem II in the S<sub>2</sub> State

Pantazis, Dimitrios A.; Ames, William; Cox, Nicholas; Lubitz, Wolfgang; Neese, Frank

doi:10.1002/anie.201204705

Cited by 368 publications

(776 citation statements)

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“…Different protonation states at W2 and O5 as well as high-and low-oxidation states of the Mn ions were assumed in the constructed models (Table 1). Model 1 (W2/O5 = H 2 O/O 2− ) and model 2 (W2/O5 = OH − /O 2− ), which both have high-oxidation states, have been used in many previous DFT and QM/MM studies (10,14,16,(18)(19)(20)22), whereas model 3 (W2/O5 = OH − /H 2 O) and model 4 (W2/O5 = H 2 O/OH − ) have low-oxidation states that previous DFT calculations suggested could fit to the 1.9-and 1.95-Å structures, respectively, revealed by X-ray crystallography (12). A model of a Ca-depleted WOC with the same protonation and oxidation states as model 1 was also calculated (model 5) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In the S 2 state, Mn 1 or Mn 4 was oxidized in the high-oxidation models, whereas Mn 2 or Mn 4 was oxidized in the low-oxidation models. The Mn 1 -and Mn 4 -oxidized S 2 states of the high-oxidation models have been proposed to reflect two conformations showing g = 4.1 and g = 2 multiline EPR signals, respectively, where the latter conformation has a slightly lower energy (10,14,17).…”

Section: Resultsmentioning

confidence: 99%

“…High-spin states were assumed in calculations. The protonation states of W2 and O5 were assumed to be H 2 O, OH − , or O 2− following previous studies (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24).…”

Section: Methodsmentioning

confidence: 99%

“…With the information of atomic coordinates from high-resolution X-ray structures of the WOC, quantum chemical calculation is now a very powerful method in investigation of the water oxidation mechanism (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme.…”

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Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Nakamura

Noguchi

2016

Proc. Natl. Acad. Sci. U.S.A.

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During photosynthesis, the light-driven oxidation of water performed by photosystem II (PSII) provides electrons necessary to fix CO 2 , in turn supporting life on Earth by liberating molecular oxygen. Recent high-resolution X-ray images of PSII show that the wateroxidizing center (WOC) is composed of an Mn 4 CaO 5 cluster with six carboxylate, one imidazole, and four water ligands. FTIR difference spectroscopy has shown significant structural changes of the WOC during the S-state cycle of water oxidation, especially within carboxylate groups. However, the roles that these carboxylate groups play in water oxidation as well as how they should be properly assigned in spectra are unresolved. In this study, we performed a normal mode analysis of the WOC using the quantum mechanics/ molecular mechanics (QM/MM) method to simulate FTIR difference spectra on the S 1 to S 2 transition in the carboxylate stretching region. By evaluating WOC models with different oxidation and protonation states, we determined that models of high-oxidation states, Mn(III) 2 Mn(IV) 2 , satisfactorily reproduced experimental spectra from intact and Ca-depleted PSII compared with low-oxidation models. It is further suggested that the carboxylate groups bridging Ca and Mn ions within this center tune the reactivity of water ligands bound to Ca by shifting charge via their π conjugation.T he oxidation of water, performed by photosystem II (PSII) in plants and cyanobacteria, is a crucial part of the photosynthesis process, providing a source of electrons used for CO 2 fixation. This process also produces molecular oxygen as a byproduct; this "waste" oxygen is released to the atmosphere, where it plays an essential role in sustaining life on Earth. The catalytic site of water oxidation is a water-oxidizing center (WOC) located in the electron-donor side of PSII (1-3). Recent high-resolution (1.9-1.95 Å) X-ray crystallographic structures of PSII (4, 5) revealed that the WOC core is an Mn 4 CaO 5 cluster fixed to the protein by six carboxylate [D1-D170, D1-E189, D1-E333, D1-D342, D1-A344 (C terminus), and CP43-E354] ligands and one imidazole (D1-H332) ligand. Four water ligands are also bound to Mn 4 (W1 and W2) and Ca (W3 and W4) (Fig. 1B shows numbering of the Mn ions and water ligands); several water molecules also exist around the Mn 4 CaO 5 cluster, forming a hydrogen bond network (Fig. 1A). Because of the absence of the information of hydrogen atoms in the X-ray structures, however, the protonation states of the water and oxo ligands in Mn 4 CaO 5 as well as the structure of the hydrogen bond network remain to be clarified.The water-oxidizing reaction proceeds through a cycle of five intermediates designated as S n states (n = 0−4) (6, 7), where S 1 is the most stable in the dark. Oxidation of the Mn 4 CaO 5 cluster by a Y Z • radical, produced by light-induced charge separation, advances the S n state (n = 0−3) to the S n + 1 state. The S 4 state immediately relaxes to the S 0 state on release of O 2 . The oxidation states of the Mn atoms wi...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Nakamura

Noguchi

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Several features of the OEC are known, including an approximate arrangement of the metal ions within the cluster (Fig. 1A) (3,4), its structural flexibility during turnover (5,6), and its ability to store oxidizing equivalents via five photo-induced redox states (S i , i = 0-4 and known as the Kok cycle) (7). Substrate water molecules bind to the cluster and, upon oxidation, are coupled to produce dioxygen and 4 eq of protons.…”

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confidence: 99%

High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Gupta

Taguchi

Lassalle‐Kaiser

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

133

162

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The structural and electronic properties of a series of manganese complexes with terminal oxido ligands are described. The complexes span three different oxidation states at the manganese center (III-V), have similar molecular structures, and contain intramolecular hydrogen-bonding networks surrounding the Mn-oxo unit. Structural studies using X-ray absorption methods indicated that each complex is mononuclear and that oxidation occurs at the manganese centers, which is also supported by electron paramagnetic resonance (EPR) studies. This gives a high-spin Mn V -oxo complex and not a Mn IV -oxy radical as the most oxidized species. In addition, the EPR findings demonstrated that the Fermi contact term could experimentally substantiate the oxidation states at the manganese centers and the covalency in the metal-ligand bonding. Oxygen-17-labeled samples were used to determine spin density within the Mn-oxo unit, with the greatest delocalization occurring within the Mn V -oxo species (0.45 spins on the oxido ligand). The experimental results coupled with density functional theory studies show a large amount of covalency within the Mn-oxo bonds. Finally, these results are examined within the context of possible mechanisms associated with photosynthetic water oxidation; specifically, the possible identity of the proposed high valent Mn-oxo species that is postulated to form during turnover is discussed.metal-oxo complexes | water oxidation | inorganic chemistry | photosynthesis | oxygen-evolving complex P hotosynthetic water oxidation is an essential chemical reaction that is responsible for producing Earth's aerobic environment. Dioxygen production occurs at the active site of the enzyme photosystem II, referred to as the oxygen-evolving complex (OEC), which contains a unique Mn 4 CaO cluster (1, 2). Several features of the OEC are known, including an approximate arrangement of the metal ions within the cluster (Fig. 1A) (3, 4), its structural flexibility during turnover (5, 6), and its ability to store oxidizing equivalents via five photo-induced redox states (S i , i = 0-4 and known as the Kok cycle) (7). Substrate water molecules bind to the cluster and, upon oxidation, are coupled to produce dioxygen and 4 eq of protons. There is agreement that formation of the O-O bond occurs in the highest oxidized state of the Mn 4 CaO 5 cluster (S 4 ), after which the cluster reverts to the most reduced state, S 0 (1-6, 8-10). The transient S 4 state has eluded detection, making it difficult to experimentally probe the structural and physical requirements necessary to promote dioxygen production. Magnetic resonance and density functional theory (DFT) studies of the S 2 and S 3 states have been used to infer that the beginning and ending oxidation states of the Kok cycle are Mn 3 III Mn IV (S 0 ) and Mn 3 IV Mn V or Mn 3 IV Mn IV O • (S 4 ) (11-14). The location of the Mn V center within the cluster is not certain, yet one possibility is the dangling Mn A4 site, which is coordinated to anionic donors and is surrounded by a ne...

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Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs

et al. 2022

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Ever since the discovery that Mn was required for oxygen evolution in plants by Pirson in 1937 and the period‐four oscillation in flash‐induced oxygen evolution by Joliot and Kok in the 1970s, understanding of this process has advanced enormously using state‐of‐the‐art methods. The most recent in this series of innovative techniques was the introduction of X‐ray free‐electron lasers (XFELs) a decade ago, which led to another quantum leap in the understanding in this field, by enabling operando X‐ray structural and X‐ray spectroscopy studies at room temperature. This review summarizes the current understanding of the structure of Photosystem II (PS II) and its catalytic centre, the Mn4CaO5 complex, in the intermediate Si (i = 0–4)‐states of the Kok cycle, obtained using XFELs.

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Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen‐Evolving Complex of Photosystem II in the S₂ State

Cited by 368 publications

References 52 publications

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs

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Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen‐Evolving Complex of Photosystem II in the S2 State

Cited by 368 publications

References 52 publications

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs

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Product

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Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen‐Evolving Complex of Photosystem II in the S₂ State

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II