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

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [1];  [3];  [1];  [2]
  1. Carnegie Mellon Univ., Pittsburgh, PA (United States). Dept. of Chemistry
  2. Univ. of California, Irvine, CA (United States). Dept. of Chemistry
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
+ Show Author Affiliations

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1235170
Alternate ID(s):
OSTI ID: 1512187
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 17; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English

References (33)

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
Structures and Energetics for O 2 Formation in Photosystem II journal December 2009
Nonheme oxo-iron(IV) intermediates form an oxyl radical upon approaching the C-H bond activation transition state journal January 2011
 -Frontier molecular orbitals in S = 2 ferryl species and elucidation of their contributions to reactivity journal August 2012
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å journal April 2011
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
Water oxidation chemistry of photosystem II journal October 2007
Biological Water Oxidation journal March 2013
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
DFT Calculations of EPR Hyperfine Coupling Tensors book May 2004
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
.sigma.-.pi. Polarization parameters for oxygen-17 in organic and inorganic .pi. radicals journal July 1973
Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms journal April 2004
Synthesis, characterization, and reactivity of oxomanganese(IV) porphyrin complexes journal December 1988
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses journal November 2014
Synthesis, Characterization, and Physicochemical Properties of Manganese(III) and Manganese(V)−Oxo Corrolazines journal June 2005
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
Structural models of the manganese complex of photosystem II and mechanistic implications journal January 2012
A water-stable manganese(V)-oxo complex: definitive assignment of a .nu.Mnv.tplbond.O infrared vibration journal January 1990
XANES Evidence Against a Manganyl Species in the S 3 State of the Oxygen-Evolving Complex journal July 2004
A proposal for water oxidation in photosystem II journal January 1998
Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S 2 State journal August 2012
Calculating the Electron Paramagnetic Resonance Parameters of Exchange Coupled Transition Metal Complexes Using Broken Symmetry Density Functional Theory:  Application to a Mn III /Mn IV Model Compound journal March 2004
Mn K-Edge X-ray Absorption Studies of Oxo- and Hydroxo-manganese(IV) Complexes: Experimental and Theoretical Insights into Pre-Edge Properties journal May 2014
Preparation and properties of an Mn IV –hydroxide complex: proton and electron transfer at a mononuclear manganese site and its relationship to the oxygen evolving complex within photosystem II journal January 2014
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
Characterization of Monomeric Mn II/III/IV –Hydroxo Complexes from X- and Q-Band Dual Mode Electron Paramagnetic Resonance (EPR) Spectroscopy journal October 2013
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
Preparation and Properties of a Monomeric Mn IV −Oxo Complex journal July 2006

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Mono‐/Multinuclear Water Oxidation Catalysts journal June 2019
Chromium Complexes with Oxido and Corrolato Ligands: Metal-Based Redox Processes versus Ligand Non-Innocence journal July 2018
Towards Catalytic Ammonia Oxidation to Dinitrogen: A Synthetic Cycle by Using a Simple Manganese Complex journal August 2017
Synthesis and Characterization of First Row Metal Complexes Derived from a Pyridinophane Ligand Functionalized by Fluoroalcohol journal March 2017
Synthesis and characterization of a flexible metal organic framework generated from Mn III and the 4,4′-bipyrazolate-ligand journal January 2018
Protic N-Heterocyclic Carbene Versus Pyrazole: Rigorous Comparison of Proton- and Electron-Donating Abilities in a Pincer-Type Framework journal September 2016
A putative heme manganese( v )-oxo species in the C–H activation and epoxidation reactions in an aqueous buffer journal January 2019
Cluster size and composition dependent water deprotonation by free manganese oxide clusters journal January 2016
How to tame a palladium terminal oxo journal January 2018
Modeling the OEC with Two New Biomimetic Models: Preparations, Structural Characterization, and Water Photolysis Studies of a Ba–Mn Box Type Complex and a Mn4N6 Planar-Diamond Cluster journal September 2018
The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S 4 state journal January 2017
Oxidation Reactions with Bioinspired Mononuclear Non-Heme Metal-Oxo Complexes journal June 2016
Structurally characterized terminal manganese( iv ) oxo tris(alkoxide) complex journal January 2018
A Manganese(V)–Oxo Tetraamido Macrocyclic Ligand (TAML) Cation Radical Complex: Synthesis, Characterization, and Reactivity Studies journal November 2018
Oxidationsreaktionen mit bioinspirierten einkernigen Nicht-Häm-Oxidometallkomplexen journal June 2016
Electrochemical C–H oxygenation and alcohol dehydrogenation involving Fe-oxo species using water as the oxygen source journal January 2019
Sizing up a supercharged ferryl journal April 2018
Low overpotential water oxidation at neutral pH catalyzed by a copper( ii ) porphyrin journal January 2019
Investigation of structural, electronic and magnetic properties of breathing metal–organic framework MIL-47(Mn): a first principles approach journal January 2020

Figures / Tables (7)

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Fig. 4(p. 6)figure Fig. 4
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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
metal–oxo complexes
water oxidation
inorganic chemistry
photosynthesis
oxygen-evolving complex