Explorations of the nonheme high-valent iron-oxo landscape: crystal structure of a synthetic complex with an [FeIV2(μ-O)2] diamond core relevant to the chemistry of sMMOH

Gregory T. Rohde; Genqiang Xue; Lawrence Que

doi:10.1039/d1fd00066g

Explorations of the nonheme high-valent iron-oxo landscape: crystal structure of a synthetic complex with an [Fe^IV₂(μ-O)₂] diamond core relevant to the chemistry of sMMOH

Gregory T. Rohde, Genqiang Xue, Lawrence Que

Chemistry (Twin Cities)

Research output: Contribution to journal › Article › peer-review

Abstract

Methanotrophic bacteria utilize methane monooxygenase (MMO) to carry out the first step in metabolizing methane. The soluble enzymes employ a hydroxylase component (sMMOH) with a nonheme diiron active site that activates O₂ and generates a powerful oxidant capable of converting methane to methanol. It is proposed that the diiron(ii) center in the reduced enzyme reacts with O₂ to generate a diferric-peroxo intermediate called P that then undergoes O-O cleavage to convert into a diiron(iv) derivative called Q, which carries out methane hydroxylation. Most (but not all) of the spectroscopic data of Q accumulated by various groups to date favor the presence of an Fe^IV₂(μ-O)₂ unit with a diamond core. The Que lab has had a long-term interest in making synthetic analogs of iron enzyme intermediates. To this end, the first crystal structure of a complex with a Fe^IIIFe^IV(μ-O)₂ diamond core was reported in 1999, which exhibited an Fe⋯Fe distance of 2.683(1) Å. Now more than 20 years later, a complex with an Fe^IV₂(μ-O)₂ diamond core has been synthesized in sufficient purity to allow diffraction-quality crystals to be grown. Its crystal structure has been solved, revealing an Fe⋯Fe distance of 2.711(4) Å for comparison with structural data for related complexes with lower iron oxidation states.

Original language	English (US)
Pages (from-to)	109-128
Number of pages	20
Journal	Faraday Discussions
Volume	234
DOIs	https://doi.org/10.1039/d1fd00066g
State	Published - Nov 5 2021

Bibliographical note

Funding Information:
We are grateful to the U. S. National Institutes of Health for support of our work via grants R01 GM-38767 and R35 GM-131721 to L. Q., Jr. XAS data were collected on beamline X3B at the National Synchrotron Radiation Light Source, which is supported by the U.S. Department of Energy under Contract No. DE-AC02-98CH10886. Use of beamline X3B was made possible by the Center for Synchrotron Biosciences grant, P30-EB-00998, from the National Institute of Biomedical Imaging and Bioengineering. Dedicated to Prof. John D. Lipscomb for his friendship and his brilliant career in studying methane monooxygenase and other nonheme iron oxygenases.

Publisher Copyright:
© 2022 The Royal Society of Chemistry

Keywords

Iron/chemistry
Methane
Oxidation-Reduction
Oxygen/chemistry
Spectrum Analysis

PubMed: MeSH publication types

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Publisher link

10.1039/d1fd00066g

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title = "Explorations of the nonheme high-valent iron-oxo landscape: crystal structure of a synthetic complex with an [FeIV2(μ-O)2] diamond core relevant to the chemistry of sMMOH",

abstract = "Methanotrophic bacteria utilize methane monooxygenase (MMO) to carry out the first step in metabolizing methane. The soluble enzymes employ a hydroxylase component (sMMOH) with a nonheme diiron active site that activates O2 and generates a powerful oxidant capable of converting methane to methanol. It is proposed that the diiron(ii) center in the reduced enzyme reacts with O2 to generate a diferric-peroxo intermediate called P that then undergoes O-O cleavage to convert into a diiron(iv) derivative called Q, which carries out methane hydroxylation. Most (but not all) of the spectroscopic data of Q accumulated by various groups to date favor the presence of an FeIV2(μ-O)2 unit with a diamond core. The Que lab has had a long-term interest in making synthetic analogs of iron enzyme intermediates. To this end, the first crystal structure of a complex with a FeIIIFeIV(μ-O)2 diamond core was reported in 1999, which exhibited an Fe⋯Fe distance of 2.683(1) {\AA}. Now more than 20 years later, a complex with an FeIV2(μ-O)2 diamond core has been synthesized in sufficient purity to allow diffraction-quality crystals to be grown. Its crystal structure has been solved, revealing an Fe⋯Fe distance of 2.711(4) {\AA} for comparison with structural data for related complexes with lower iron oxidation states.",

keywords = "Iron/chemistry, Methane, Oxidation-Reduction, Oxygen/chemistry, Spectrum Analysis",

author = "Rohde, {Gregory T.} and Genqiang Xue and Lawrence Que",

note = "Funding Information: We are grateful to the U. S. National Institutes of Health for support of our work via grants R01 GM-38767 and R35 GM-131721 to L. Q., Jr. XAS data were collected on beamline X3B at the National Synchrotron Radiation Light Source, which is supported by the U.S. Department of Energy under Contract No. DE-AC02-98CH10886. Use of beamline X3B was made possible by the Center for Synchrotron Biosciences grant, P30-EB-00998, from the National Institute of Biomedical Imaging and Bioengineering. Dedicated to Prof. John D. Lipscomb for his friendship and his brilliant career in studying methane monooxygenase and other nonheme iron oxygenases. Publisher Copyright: {\textcopyright} 2022 The Royal Society of Chemistry",

year = "2021",

month = nov,

day = "5",

doi = "10.1039/d1fd00066g",

language = "English (US)",

volume = "234",

pages = "109--128",

journal = "Faraday Discussions",

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AU - Rohde, Gregory T.

AU - Xue, Genqiang

AU - Que, Lawrence

N1 - Funding Information: We are grateful to the U. S. National Institutes of Health for support of our work via grants R01 GM-38767 and R35 GM-131721 to L. Q., Jr. XAS data were collected on beamline X3B at the National Synchrotron Radiation Light Source, which is supported by the U.S. Department of Energy under Contract No. DE-AC02-98CH10886. Use of beamline X3B was made possible by the Center for Synchrotron Biosciences grant, P30-EB-00998, from the National Institute of Biomedical Imaging and Bioengineering. Dedicated to Prof. John D. Lipscomb for his friendship and his brilliant career in studying methane monooxygenase and other nonheme iron oxygenases. Publisher Copyright: © 2022 The Royal Society of Chemistry

PY - 2021/11/5

Y1 - 2021/11/5

N2 - Methanotrophic bacteria utilize methane monooxygenase (MMO) to carry out the first step in metabolizing methane. The soluble enzymes employ a hydroxylase component (sMMOH) with a nonheme diiron active site that activates O2 and generates a powerful oxidant capable of converting methane to methanol. It is proposed that the diiron(ii) center in the reduced enzyme reacts with O2 to generate a diferric-peroxo intermediate called P that then undergoes O-O cleavage to convert into a diiron(iv) derivative called Q, which carries out methane hydroxylation. Most (but not all) of the spectroscopic data of Q accumulated by various groups to date favor the presence of an FeIV2(μ-O)2 unit with a diamond core. The Que lab has had a long-term interest in making synthetic analogs of iron enzyme intermediates. To this end, the first crystal structure of a complex with a FeIIIFeIV(μ-O)2 diamond core was reported in 1999, which exhibited an Fe⋯Fe distance of 2.683(1) Å. Now more than 20 years later, a complex with an FeIV2(μ-O)2 diamond core has been synthesized in sufficient purity to allow diffraction-quality crystals to be grown. Its crystal structure has been solved, revealing an Fe⋯Fe distance of 2.711(4) Å for comparison with structural data for related complexes with lower iron oxidation states.

AB - Methanotrophic bacteria utilize methane monooxygenase (MMO) to carry out the first step in metabolizing methane. The soluble enzymes employ a hydroxylase component (sMMOH) with a nonheme diiron active site that activates O2 and generates a powerful oxidant capable of converting methane to methanol. It is proposed that the diiron(ii) center in the reduced enzyme reacts with O2 to generate a diferric-peroxo intermediate called P that then undergoes O-O cleavage to convert into a diiron(iv) derivative called Q, which carries out methane hydroxylation. Most (but not all) of the spectroscopic data of Q accumulated by various groups to date favor the presence of an FeIV2(μ-O)2 unit with a diamond core. The Que lab has had a long-term interest in making synthetic analogs of iron enzyme intermediates. To this end, the first crystal structure of a complex with a FeIIIFeIV(μ-O)2 diamond core was reported in 1999, which exhibited an Fe⋯Fe distance of 2.683(1) Å. Now more than 20 years later, a complex with an FeIV2(μ-O)2 diamond core has been synthesized in sufficient purity to allow diffraction-quality crystals to be grown. Its crystal structure has been solved, revealing an Fe⋯Fe distance of 2.711(4) Å for comparison with structural data for related complexes with lower iron oxidation states.

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KW - Methane

KW - Oxidation-Reduction

KW - Oxygen/chemistry

KW - Spectrum Analysis

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