Two-dimensional 14N HYSCORE spectroscopy of the coordination geometry of ligands in dimanganese di-μ-oxo mimics of the oxygen evolving complex of photosystem II

Chatterjee, Ruchira; Milikisiyants, Sergey; Lakshmi, K. V.

doi:10.1039/c2cp40416h

Cited by 10 publications

(14 citation statements)

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“…In the present study, we use two-dimensional (2D) hyperfine sublevel correlation (HYSCORE) spectroscopy (see Transparent Methods ) to obtain a quantitative measure of the hyperfine and quadrupolar parameters of the BiP–PF 10 ⋅+ radical ( Chatterjee et al., 2013 , 2012 ; Coates et al., 2015 ; Dikanov et al., 2019 , 2000 ; Dikanov and Taguchi, 2018 ; Höfer et al., 1986 ; Milikisiyants et al., 2011 , 2010 ). 2D HYSCORE spectroscopy is similar to the pulsed EPR spectroscopy methods, electron nuclear double resonance (ENDOR), and electron spin echo envelope modulation (ESEEM) ( Britt, 2003 ; Deligiannakis et al., 2000 ; Harmer et al, 2009 ; Lakshmi and Brudvig, 2001 ; Prisner et al., 2001 ), that are used for the study of electron-nuclear hyperfine interactions in paramagnetic systems.…”

Section: Resultsmentioning

confidence: 99%

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

et al. 2020

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Summary The photosynthetic water-oxidation reaction is catalyzed by the oxygen-evolving complex in photosystem II (PSII) that comprises the Mn 4 CaO 5 cluster, with participation of the redox-active tyrosine residue (Y Z ) and a hydrogen-bonded network of amino acids and water molecules. It has been proposed that the strong hydrogen bond between Y Z and D1-His190 likely renders Y Z kinetically and thermodynamically competent leading to highly efficient water oxidation. However, a detailed understanding of the proton-coupled electron transfer (PCET) at Y Z remains elusive owing to the transient nature of its intermediate states involving Y Z ⋅. Herein, we employ a combination of high-resolution two-dimensional 14 N hyperfine sublevel correlation spectroscopy and density functional theory methods to investigate a bioinspired artificial photosynthetic reaction center that mimics the PCET process involving the Y Z residue of PSII. Our results underscore the importance of proximal water molecules and charge delocalization on the electronic structure of the artificial reaction center.

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Section: Resultsmentioning

confidence: 99%

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

et al. 2020

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“…The details of the spectrometer are described in previous literature. 32,33,[41][42][43][44] All of the pulsed EPR spectra were acquired at 5 K.…”

Section: Pulsed Epr Spectroscopymentioning

confidence: 99%

The structure and activation of substrate water molecules in Sr²⁺-substituted photosystem II

Chatterjee

Milikisiyants

Coates

et al. 2014

Phys. Chem. Chem. Phys.

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The mechanism of solar water oxidation by photosystem II (PSII) is of fundamental interest and it is the object of extensive studies both in the past and present. The solar water oxidation reaction of PSII occurs in the oxygen-evolving complex (OEC). The OEC consists of a tetranuclear manganese calcium-oxo (Mn4Ca-oxo) cluster that is surrounded by amino acid residues and inorganic cofactors. The role of the Ca(2+) ion in the water oxidation reaction is one of the most interesting questions that is yet to be answered. In this study, we probe the structural and functional differences induced by metal ion substitution in the Mn4Ca-oxo cluster by substituting the Ca(2+) ion in the OEC by a Sr(2+) ion. We apply two-dimensional (2D) hyperfine sublevel correlation (HYSCORE) spectroscopy to detect weak magnetic interactions between the paramagnetic Mn4Sr-oxo cluster and the surrounding protons in the S2 state of the OEC of Sr(2+)-substituted PSII. We identify three groups of protons that are magnetically interacting with the Mn4Sr-oxo cluster. Using the recently reported 1.9 Å resolution X-ray structure of the OEC in the S1 state [Umena et al.] and the high-resolution 2D HYSCORE spectroscopy studies of the S2 state of the OEC of Ca(2+)-containing PSII [Milikisiyants et al., Energy Environ. Sci., 2012, 5, 7747], we discuss the assignments of the three groups of protons that are magnetically coupled to the Mn4Sr-oxo cluster. Since hyperfine interactions are highly sensitive to small perturbations in the electronic and geometric structure of paramagnetic centers, a comparison of the 2D HYSCORE spectra of Sr(2+)-substituted and Ca(2+)-containing PSII allows us to draw important conclusions with respect to the structure of the substrate water molecules in the OEC and the role of the Ca(2+) ion in the water oxidation reaction. In addition, for the first time, we determine the experimental value of the spin projection factor for the Mn(III) ion of the Mn4Ca-oxo cluster as ρ1 = ±1.7 from the assignment of the hyperfine interaction of the paramagnetic cluster with the protons of the D1-His332 residue of PSII.

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“…In the present study, we use two-dimensional (2D) hyperfine sublevel correlation (HYSCORE) spectroscopy to obtain a quantitative measure of the hyperfine and quadrupolar parameters of the BiP-PF10 •+ radical. [51][52][53][54][55][56][57][58][59] 2D HYSCORE spectroscopy is similar to the pulsed EPR spectroscopy methods, electron nuclear double resonance (ENDOR) and electron spin echo envelope modulation (ESEEM), [60][61][62][63][64] that are used for the study of electron-nuclear hyperfine interactions in paramagnetic systems. However, in comparison with the other methods the observation of HYSCORE signals in twodimensional (2D) frequency space results in enhanced resolution, which alleviates the problem of spectral overcrowding from the simultaneous detection of multiple nuclear spins, 62 such as, the nitrogen atoms of the BiP-PF10 •+ radical.…”

Section: Resultsmentioning

confidence: 99%

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

Méndez-Hernández

Baldansuren²,

Kalendra³

et al. 2020

Preprint

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Light-driven water oxidation in algae, cyanobacteria, and higher plants generates dioxygen that supports life on Earth. The water-oxidation reaction is catalyzed by the oxygen-evolving complex (OEC) in photosystem II (PSII) that is comprised of the tetranuclear manganese calcium-oxo (Mn4CaO5) cluster, with participation of the redox-active tyrosine residue (YZ) and a hydrogen-bonded network of amino acids and water molecules. YZ mediates successive proton-coupled electron transfer (PCET) reactions that are essential for the oxidation of water to dioxygen at the Mn4CaO5 cluster. It has been proposed that the strong hydrogen bond between YZ and and its conjugate base, D1-His190, likely renders YZ kinetically and thermodynamically competent leading to highly efficient water oxidation.1 However, a detailed understanding of PCET at YZ remains elusive due to the transient nature of its intermediate states. In this study, we utilize a combination of high-resolution two-dimensional (2D) 14N hyperfine sublevel correlation (HYSCORE) spectroscopy and density functional theory (DFT) methods to investigate the electronic structure of a bioinspired artificial photosynthetic reaction center, benzimidazole-phenol porphyrin (BiP–PF10), that mimics the PCET process at the YZ residue of PSII. The results of these studies underscore the importance of proximal water molecules and charge delocalization on the electronic structure of the artificial reaction center.

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Two-dimensional 14N HYSCORE spectroscopy of the coordination geometry of ligands in dimanganese di-μ-oxo mimics of the oxygen evolving complex of photosystem II

Cited by 10 publications

References 49 publications

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

The structure and activation of substrate water molecules in Sr²⁺-substituted photosystem II

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

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Two-dimensional 14N HYSCORE spectroscopy of the coordination geometry of ligands in dimanganese di-μ-oxo mimics of the oxygen evolving complex of photosystem II

Cited by 10 publications

References 49 publications

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

The structure and activation of substrate water molecules in Sr2+-substituted photosystem II

HYSCORE and DFT Studies of Proton-Coupled Electron Transfer in a Bioinspired Artificial Photosynthetic Reaction Center

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The structure and activation of substrate water molecules in Sr²⁺-substituted photosystem II