X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme

Ono, T.; Noguchi, Takumi; Inoue, Yorinao; Kusunoki, Masami; Matsushita, Tadashi; Ōyanagi, H.

doi:10.1126/science.258.5086.1335

Cited by 218 publications

(232 citation statements)

References 21 publications

Supporting

Mentioning

207

Contrasting

Unclassified

Order By: Relevance

“…Mn(1)ZIV, Mn(2)ZIV, Mn(3)ZIII, Mn(4)ZIII) and model (b) where an additional water ligand is completing the hexacoordinated shell of Mn(4) and the oxidation states are Mn 4 (IV,III,III,IV ). These results are partially consistent with EPR and X-ray spectroscopic evidence (Ono et al 1992;Yachandra et al 1993;Roelofs et al 1996;Bergmann et al 1998;Iuzzolino et al 1998;Dau et al 2001;Messinger et al 2001) but disagree with the suggested low-valent Mn 4 (III,III,III,III ) state (Zheng & Dismukes 1996;Kuzek & Pace 2001).…”

Section: Structural Models Of the O 2 -Evolving Centresupporting

confidence: 73%

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Sproviero

Shinopoulos

Gascón

et al. 2007

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

This paper reports computational studies of substrate water binding to the oxygen-evolving centre (OEC) of photosystem II (PSII ), completely ligated by amino acid residues, water, hydroxide and chloride. The calculations are based on quantum mechanics/molecular mechanics hybrid models of the OEC of PSII, recently developed in conjunction with the X-ray crystal structure of PSII from the cyanobacterium Thermosynechococcus elongatus. The model OEC involves a cuboidal Mn 3 CaO 4 Mn metal cluster with three closely associated manganese ions linked to a single m 4 -oxo-ligated Mn ion, often called the 'dangling manganese'. Two water molecules bound to calcium and the dangling manganese are postulated to be substrate molecules, responsible for dioxygen formation. It is found that the energy barriers for the Mn(4)-bound water agree nicely with those of model complexes. However, the barriers for Ca-bound waters are substantially larger. Water binding is not simply correlated to the formal oxidation states of the metal centres but rather to their corresponding electrostatic potential atomic charges as modulated by charge-transfer interactions. The calculations of structural rearrangements during water exchange provide support for the experimental finding that the exchange rates with bulk 18 O-labelled water should be smaller for water molecules coordinated to calcium than for water molecules attached to the dangling manganese. The models also predict that the S 1 /S 2 transition should produce opposite effects on the two waterexchange rates.

show abstract

Section: Structural Models Of the O 2 -Evolving Centresupporting

confidence: 73%

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Sproviero

Shinopoulos

Gascón

et al. 2007

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

show abstract

“…However, on the basis of Mn K-edge studies, other groups have proposed that Mn is oxidized during the S 0 →S 1 , S 1 →S 2 , and also during the S 2 →S 3 transitions. 17,18 The requirement of a higher signal-to-noise ratio for the EXAFS relative to the XANES experiments has made EXAFS measurements more difficult for the flash-induced S state samples. Earlier EXAFS data from the chemically treated S 3 state samples produced by a double-turnover method indicated that the two di-μ-oxo-bridged Mn-Mn dimer units may become nonequivalent.…”

Section: Introductionmentioning

confidence: 99%

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

et al. 2000

View full text Add to dashboard Cite

The oxygen-evolving complex of Photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S 0 -S 4 ) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the Photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S 1 and S 2 states. The proposed model consists of two di-μ-oxo-bridged binuclear Mn units with Mn-Mn distances of ~2.7 Å that are linked to each other by a mono-μ-oxo bridge with a Mn-Mn separation of ~3.3 Å. The Mn-Mn distances are invariant in the native S 1 and S 2 states. This report describes the application of X-ray absorption spectroscopy to S 3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S 3 state compared to the S 1 and the S 2 states. The two 2.7 Å Mn-Mn distances that characterize the di-μ-oxo centers in the S 1 and S 2 states are lengthened to ~2.8 and 3.0 Å in the S 3 state, respectively. The 3.3 Å Mn-Mn and Mn-Ca distances also increase by 0.04-0.2 Å. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S 3 state. Mn-centered oxidation is evident during the S 0 →S 1 and S 1 →S 2 transitions. We propose that the changes in Mn-Mn distances during the S 2 →S 3 transition are the result of ligand or water oxidation, leading to the Supporting Information Available: E-space S 3 state EXAFS spectrum; the data in k-space and the background that was removed to reduce the low-frequency contributions that show up as peaks at <1 Å in the Fourier transform; and the Fourier isolate of the k-space S 3 spectrum, shown overplotted on the S 3 EXAFS spectrum (PDF). This material is available free of charge via the Internet at http:// pubs.acs.org. NIH Public Access

show abstract

“…119 Mn K-edge x-ray absorption near edge structure (XANES) has been used to probe the Mn valence at the different S states. 19,20,115,141 The Mn K-edge positions for the S 0 , S 1 and S 2 states have been determined as inflection-point energies from second derivative zero-crossings 142 and the overall edge shape is consistent with oxygen ligation. 107 The shifts in edge position, along with characteristic changes in the edge shapes are indicative of Mn oxidation, so that the proposed Mn oxidation state assignments are as follows: S 0 (II, III, IV, IV) or (III, III, III, IV), S 1 (III, III, IV, IV), and S 2 (III, IV, IV, IV).…”

Section: Introductionmentioning

confidence: 99%

“…Much has been learned about the catalytic Mn cluster, and a working model has been proposed 11,[16][17][18] based mainly on X-ray absorption spectroscopy (XAS) and electron paramagnetic resonance (EPR) studies. Both X-ray absorption near-edge structure (XANES) and extended X-ray absorption fine structure (EXAFS) experiments have focused on the Mn atoms of the OEC to obtain oxidation states, 19,20 and structural information about this active site. [21][22][23][24][25][26] Along with manganese and chloride, Ca is an essential cofactor in oxygen evolution.…”

Section: Introductionmentioning

confidence: 99%

“…11,[107][108][109] Without the benefit of suitable crystals for high-resolution x-ray crystallography, 110,111 x-ray absorption spectroscopy (XAS) 7,25,59,61 and electron paramagnetic resonance (EPR) [112][113][114] studies have emerged as the primary methods to provide structural and chemical information about the OEC and devise a working model for its manganese cluster. Because these methods are element-specific and sensitive at dilute concentrations, x-ray absorption near-edge structure (XANES) 19,20,115 and extended x-ray absorption fine structure (EXAFS) [22][23][24][25]46 analyses have been applied at the Mn K-edge to determine oxidation states and information about the local environment of the Mn atoms.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

X-ray absorption spectroscopy on the calcium cofactor to the manganese cluster in photosynthetic oxygen evolution

Cinco¹

1999

View full text Add to dashboard Cite

PS II). To further test and verify whetherCa is close to the Mn cluster, we substituted strontium for Ca and probed from the Sr point of view for any nearby Mn. The extended X-ray absorption fine structure (EXAFS) of Sr-reactivated PS II indicates major differences between the intact and NH 2 OH-treated samples. In intact samples, the Fourier transform of the Sr EXAFS shows a Fourier peak that is missing in inactive samples. This peak II is best simulated by two Mn neighbors at a distance of 3.5 Å, confirming the proximity of Ca (Sr) cofactor to the Mn cluster. In addition, polarized Sr EXAFS on oriented Sr-reactivated samples shows this peak II is dichroic: large magnitude at 10° (angle between the PS II membrane normal and the x-ray electric field vector) and small at 80°. Analysis of the dichroism yields the relative angle between the Sr-Mn vector and membrane normal (23° ± 4°), and the isotropic coordination number for these layered samples.ii X-ray absorption spectroscopy has also been employed to assess the degree of similarity between the manganese cluster in 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). 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 EXAFS method detects the small changes in the core structures as X is varied in this series, and serves to exclude these distorted cubanes of C 3v symmetry as a topological model for the Mn catalytic cluster.The sulfur K-edge x-ray absorption near-edge structure (XANES) spectra for the amino acids cysteine, methionine, their corresponding oxidized forms cystine and methionine sulfoxide, and glutathione show distinct differences between the thiol and disulfide forms. Sulfur XANES is also used to detect changes (within 5%) of the thiol-to-disulfide ratio in whole human blood, plasma, and erythrocytes.iii To my parents, and to my brothers Raoul and Dannyi v

show abstract

X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme

Cited by 218 publications

References 21 publications

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

X-ray absorption spectroscopy on the calcium cofactor to the manganese cluster in photosynthetic oxygen evolution

Contact Info

Product

Resources

About

X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme

Cited by 218 publications

References 21 publications

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Structural Change of the Mn Cluster during the S2→S3 State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

X-ray absorption spectroscopy on the calcium cofactor to the manganese cluster in photosynthetic oxygen evolution

Contact Info

Product

Resources

About

Structural Change of the Mn Cluster during the S₂→S₃ State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy