Mn<sub>4</sub>Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen

Yano, Junko; Yachandra, Vittal K.

doi:10.1021/cr4004874

Cited by 593 publications

(643 citation statements)

References 235 publications

(590 reference statements)

Supporting

Mentioning

616

Contrasting

Unclassified

Order By: Relevance

“…oxygenases) and synthetic oxidation catalysts. [1][2][3][4][5] Many examples of natural and synthetic terminal high-valent Fe-oxygen, and Mn-oxygen species have been reported in the last decade. 6,7 In sharp contrast, and despite some efforts, detection of terminal high-valent metal-oxygen species involved in the mode of action of highly efficient oxidation catalysts based on late-transition metals such as cobalt, nickel or copper are scarce.…”

Section: Introductionmentioning

confidence: 99%

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

et al. 2016

View full text Add to dashboard Cite

Abstract.Terminal high-valent metal-oxygen species are key reaction intermediates in the catalytic cycle of both enzymes (e.g., oxygenases) and synthetic oxidation catalysts. While tremendous efforts have been directed towards the characterization of the biologically relevant terminal manganese-oxygen and iron-oxygen species, the corresponding analogues based on late-transition metals such as cobalt, nickel or copper are relatively scarce. This is in part related to the "Oxo Wall" concept, which predicts that late transition elements cannot support a terminal oxido ligand in a tetragonal environment. Here, the nickel(II) complex (1) of the tetradentate macrocyclic ligand bearing a 2,6-pyridinedicarboxamidate unit is shown to be an effective catalyst in the chlorination and oxidation of C-H bonds with sodium hypochlorite as terminal oxidant in the presence of acetic acid (AcOH). Insight into the active species responsible for the observed reactivity was gained through the study of the reaction of 1 with ClO -at low temperature by UV/Vis absorption, resonance Raman, EPR, ESI-MS, and XAS analyses. DFT calculations aided the assignment of the trapped chromophoric species (3) as a nickel-hypochlorite species. Despite the fact that the formal oxidation state of the nickel in 3 is +4, experimental and computational analysis indicate that 3 is best formulated as a Ni III complex with one unpaired electron delocalized in the ligands surrounding the metal center. Most remarkably, 3 reacts rapidly with a range of substrates including those with strong aliphatic C-H bonds, indicating the direct involvement of 3 in the oxidation/chlorination reactions observed in the 1/ClO -

show abstract

Section: Introductionmentioning

confidence: 99%

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

et al. 2016

View full text Add to dashboard Cite

show abstract

“…

…”

mentioning

confidence: 99%

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

Suga

Akita

Sugahara

et al. 2017

Nature

539

791

View full text Add to dashboard Cite

SummaryPhotosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer, and catalyzes light-driven water oxidation at its catalytic center, the oxygen-evolving complex (OEC) [1][2][3] . The structure of PSII has been analyzed at 1.9 Å resolution by synchrotron radiation X-rays, which revealed that OEC is a Mn4CaO5 cluster organized in an asymmetric, "distorted-chair" form 4 . This structure was further analyzed with femtosecond X-ray free electron lasers (XFEL), providing the "radiation damage-free" 5 structure. The mechanism of O=O bond formation, however, remains obscure due to the lack of intermediate state structures. Here we report the structural changes of PSII induced by 2-flash (2F) illumination at room temperature at a resolution of 2.35 Å using time-resolved serial femtosecond crystallography (TR-SFX) with an XFEL provided by the SPring-8 angstrom compact free-electron laser (SACLA). Isomorphous differenceFourier map between the 2F and dark-adapted states revealed two areas of apparent changes; they are around QB/non-heme iron and the Mn4CaO5 cluster. The changes around the QB/non-heme iron region reflected the electron and proton transfers induced by the 2F-illumination. In the region around the Mn4CaO5 cluster, a water molecule located 3.5 Å from the Mn4CaO5 cluster disappeared from the map upon 2Fillumination, leading to a closer distance between another water molecule and O4, suggesting also the occurrence of proton transfer. Importantly, the 2F-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ3-oxo-bridge located in the quasi-center of Mn1 and Mn4 4,5 . This suggests an insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 Å between these two oxygen atoms. This provides a mechanism for the O=O bond formation 4 consistent with that proposed by Siegbahn 6,7 . Fig. 1a shows organization of the electron transfer chain of PSII in a pseudo-C2 symmetry by two subunits D1 and D2. The water-oxidation reaction proceeds via the Si-state cycle 8 (with i=0-4), where dioxygen is produced in the transition of S3→(S4)→S0 (Fig. 1b). The high-resolution structures of PSII analyzed so far were for the dark-stable S1 state 4,5 , although a few studies on the low-resolution intermediate S-state structures have been reported by TR-SFX [9][10][11] . During the revision of our manuscript, Young et al. reported a 2F-illuminated state structure at 2.25 Å resolution where no apparent changes around O5 were observed 12 , although estimations of the resolution could yield somewhat different values so that small movement of some water molecules may escape the detection. In order to achieve resolution high enough to uncover small structural changes induced by flash illuminations yet allowing Si-state transition to proceed efficiently, we determined the optimal crystal size of PSII with a maximum length of 100 µm, which diffracted up to a resolution of 2.1 Å by a SACLA-XFEL ...

show abstract

“…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)(2)(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.…”

mentioning

confidence: 99%

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.

View full text Add to dashboard Cite

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...

show abstract

Mn₄Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen

Cited by 593 publications

References 235 publications

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

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

Contact Info

Product

Resources

About

Mn4Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen

Cited by 593 publications

References 235 publications

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

Rapid Hydrogen and Oxygen Atom Transfer by a High-Valent Nickel–Oxygen Species

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

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

Contact Info

Product

Resources

About

Mn₄Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen

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