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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 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 formmore » during turnover is discussed.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (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 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.},
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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Publisher's Version of Record
https://doi.org/10.1073/pnas.1422800112
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Cited by: 35 works
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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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Works referenced in this record:

Detection of the Water-Binding Sites of the Oxygen-Evolving Complex of Photosystem II Using W-Band 17 O Electron–Electron Double Resonance-Detected NMR Spectroscopy
journal, September 2012

  • Rapatskiy, Leonid; Cox, Nicholas; Savitsky, Anton
  • Journal of the American Chemical Society, Vol. 134, Issue 40
  • DOI: 10.1021/ja3053267

Biological Water Oxidation
journal, March 2013

  • Cox, Nicholas; Pantazis, Dimitrios A.; Neese, Frank
  • Accounts of Chemical Research, Vol. 46, Issue 7
  • DOI: 10.1021/ar3003249

Theoretical Evaluation of Structural Models of the S 2 State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions
journal, December 2011

  • Ames, William; Pantazis, Dimitrios A.; Krewald, Vera
  • Journal of the American Chemical Society, Vol. 133, Issue 49
  • DOI: 10.1021/ja2041805

Utilization of Hydrogen Bonds To Stabilize M−O(H) Units:  Synthesis and Properties of Monomeric Iron and Manganese Complexes with Terminal Oxo and Hydroxo Ligands
journal, February 2004

  • MacBeth, Cora E.; Gupta, Rajeev; Mitchell-Koch, Katie R.
  • Journal of the American Chemical Society, Vol. 126, Issue 8
  • DOI: 10.1021/ja0305151

.sigma.-.pi. Polarization parameters for oxygen-17 in organic and inorganic .pi. radicals
journal, July 1973

  • Melamud, E.; Silver, Brian L.
  • The Journal of Physical Chemistry, Vol. 77, Issue 15
  • DOI: 10.1021/j100634a016

Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms
journal, April 2004

  • Britt, R. David; Campbell, Kristy A.; Peloquin, Jeffrey M.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1655
  • DOI: 10.1016/j.bbabio.2003.11.009

Synthesis, characterization, and reactivity of oxomanganese(IV) porphyrin complexes
journal, December 1988

  • Groves, John T.; Stern, Michael K.
  • Journal of the American Chemical Society, Vol. 110, Issue 26
  • DOI: 10.1021/ja00234a009

Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses
journal, November 2014

  • Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio
  • Nature, Vol. 517, Issue 7532
  • DOI: 10.1038/nature13991

Structures and Energetics for O 2 Formation in Photosystem II
journal, December 2009

  • Siegbahn, Per E. M.
  • Accounts of Chemical Research, Vol. 42, Issue 12
  • DOI: 10.1021/ar900117k

Synthesis, Characterization, and Physicochemical Properties of Manganese(III) and Manganese(V)−Oxo Corrolazines
journal, June 2005

  • Lansky, David E.; Mandimutsira, Beaven; Ramdhanie, Bobby
  • Inorganic Chemistry, Vol. 44, Issue 13
  • DOI: 10.1021/ic0503636

The calcium and chloride requirements of the O2 evolving complex
journal, February 2008

Preparation and Properties of a Monomeric High-Spin Mn V –Oxo Complex
journal, January 2012

  • Taguchi, Taketo; Gupta, Rupal; Lassalle-Kaiser, Benedikt
  • Journal of the American Chemical Society, Vol. 134, Issue 4
  • DOI: 10.1021/ja210957u

Structural models of the manganese complex of photosystem II and mechanistic implications
journal, January 2012

  • Grundmeier, Alexander; Dau, Holger
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.07.004

A water-stable manganese(V)-oxo complex: definitive assignment of a .nu.Mnv.tplbond.O infrared vibration
journal, January 1990

  • Collins, Terrence J.; Powell, Richard D.; Slebodnick, Carla
  • Journal of the American Chemical Society, Vol. 112, Issue 2
  • DOI: 10.1021/ja00158a077

Nonheme oxo-iron(IV) intermediates form an oxyl radical upon approaching the C-H bond activation transition state
journal, January 2011

  • Ye, S.; Neese, F.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
  • DOI: 10.1073/pnas.1008411108

 -Frontier molecular orbitals in S = 2 ferryl species and elucidation of their contributions to reactivity
journal, August 2012

  • Srnec, M.; Wong, S. D.; England, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 36
  • DOI: 10.1073/pnas.1212693109

XANES Evidence Against a Manganyl Species in the S 3 State of the Oxygen-Evolving Complex
journal, July 2004

  • Weng, Tsu-Chien; Hsieh, Wen-Yuan; Uffelman, Erich S.
  • Journal of the American Chemical Society, Vol. 126, Issue 26
  • DOI: 10.1021/ja0494104

A proposal for water oxidation in photosystem II
journal, January 1998

  • Pecoraro, V. L.; Baldwin, M. J.; Caudle, M. T.
  • Pure and Applied Chemistry, Vol. 70, Issue 4
  • DOI: 10.1351/pac199870040925

Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S 2 State
journal, August 2012

  • Pantazis, Dimitrios A.; Ames, William; Cox, Nicholas
  • Angewandte Chemie International Edition, Vol. 51, Issue 39
  • DOI: 10.1002/anie.201204705

Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011

  • Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09913

Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn4Ca Cluster
journal, November 2006

Spectroscopic Characterization of Inhibitor Interactions with the Mn(III)/Mn(IV) Core in Lactobacillus plantarum Manganese Catalase
journal, October 1997

  • Stemmler, Timothy L.; Sturgeon, Bradley E.; Randall, David W.
  • Journal of the American Chemical Society, Vol. 119, Issue 39
  • DOI: 10.1021/ja9704040

Water oxidation chemistry of photosystem II
journal, October 2007

  • Brudvig, Gary W.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494
  • DOI: 10.1098/rstb.2007.2217

Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation
journal, August 2014

COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970

Polarized X-ray Absorption Spectroscopy of Single-Crystal Mn(V) Complexes Relevant to the Oxygen-Evolving Complex of Photosystem II
journal, October 2007

  • Yano, Junko; Robblee, John; Pushkar, Yulia
  • Journal of the American Chemical Society, Vol. 129, Issue 43
  • DOI: 10.1021/ja071286b

Characterization of Monomeric Mn II/III/IV –Hydroxo Complexes from X- and Q-Band Dual Mode Electron Paramagnetic Resonance (EPR) Spectroscopy
journal, October 2013

  • Gupta, Rupal; Taguchi, Taketo; Borovik, A. S.
  • Inorganic Chemistry, Vol. 52, Issue 21
  • DOI: 10.1021/ic401681r

Hyperfine Coupling to the Bridging 17 O in the Di-μ-oxo Core of a Mn III −Mn IV Model Significant to the Core Electronic Structure of the O 2 -Evolving Complex in Photosystem II
journal, October 2007

  • Usov, Oleg M.; Grigoryants, Vladimir M.; Tagore, Ranitendranath
  • Journal of the American Chemical Society, Vol. 129, Issue 39
  • DOI: 10.1021/ja073179n

Preparation and Properties of a Monomeric Mn IV −Oxo Complex
journal, July 2006

  • Parsell, Trenton H.; Behan, Rachel K.; Green, Michael T.
  • Journal of the American Chemical Society, Vol. 128, Issue 27
  • DOI: 10.1021/ja062332v
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