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

Abstract

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 MnV–oxo complex and not a MnIV–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 MnV–oxo species (0.45 spins on the oxido ligand). Here, 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.

Authors:
 [1];  [2];  [3];  [1];  [3];  [1];  [2]
+ Show Author Affiliations
  1. Department of Chemistry, Carnegie Mellon University, Pittsburgh, PA 15213,
  2. Department of Chemistry, University of California, Irvine, CA 92697, and
  3. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1235170
Alternate Identifier(s):
OSTI ID: 1512187
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 17; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; metal–oxo complexes; water oxidation; inorganic chemistry; photosynthesis; oxygen-evolving complex

Citation Formats

Gupta, Rupal, Taguchi, Taketo, Lassalle-Kaiser, Benedikt, Bominaar, Emile L., Yano, Junko, Hendrich, Michael P., and Borovik, A. S.. High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II. United States: N. p., 2015. Web. doi:10.1073/pnas.1422800112.
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Gupta, Rupal, Taguchi, Taketo, Lassalle-Kaiser, Benedikt, Bominaar, Emile L., Yano, Junko, Hendrich, Michael P., & Borovik, A. S.. High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II. United States. https://doi.org/10.1073/pnas.1422800112
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Gupta, Rupal, Taguchi, Taketo, Lassalle-Kaiser, Benedikt, Bominaar, Emile L., Yano, Junko, Hendrich, Michael P., and Borovik, A. S.. Tue . "High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II". United States. https://doi.org/10.1073/pnas.1422800112.
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@article{osti_1235170,
title = {High-spin Mn–oxo complexes and their relevance to the oxygen-evolving complex within photosystem II},
author = {Gupta, Rupal and Taguchi, Taketo and Lassalle-Kaiser, Benedikt and Bominaar, Emile L. and Yano, Junko and Hendrich, Michael P. and Borovik, A. S.},
abstractNote = {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 MnV–oxo complex and not a MnIV–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 MnV–oxo species (0.45 spins on the oxido ligand). Here, 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.},
doi = {10.1073/pnas.1422800112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 17,
volume = 112,
place = {United States},
year = {2015},
month = {4}
}
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Journal Article:
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https://doi.org/10.1073/pnas.1422800112
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Figures / Tables:

Fig. 1 Fig. 1: (A–D) Structures of the OEC cluster illustrating the hydrogen-bonding network (A) (purple spheres, Mn; light blue spheres, Ca2+; red spheres, oxido/ hydroxo ligands; blue sphere, nitrogen; white spheres, water), the nucleophilic mechanism for O–O bond formation (B), the radical coupling mechanism for O–O bond formation (C), and themore » Mn–oxo complexes used in this study (D). The structure in A is adapted from Protein Data Bank ID 3BZ1.« less
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