High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

Rebeca G. Castillo; Rahul Banerjee; Caleb J. Allpress; Gregory T. Rohde; Eckhard Bill; Lawrence Que; John D. Lipscomb; Serena DeBeer

doi:10.1021/jacs.7b09560

High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

Rebeca G. Castillo, Rahul Banerjee, Caleb J. Allpress, Gregory T. Rohde, Eckhard Bill, Lawrence Que, John D. Lipscomb, Serena DeBeer

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Abstract

Kα high-energy-resolution fluorescence detected X-ray absorption spectroscopy (HERFD XAS) provides a powerful tool for overcoming the limitations of conventional XAS to identify the electronic structure and coordination environment of metalloprotein active sites. Herein, Fe Kα HERFD XAS is applied to the diiron active site of soluble methane monooxygenase (sMMO) and to a series of high-valent diiron model complexes, including diamond-core [Fe^IV₂(μ-O)₂(L)₂](ClO₄)₄] (3) and open-core [(O=Fe^IV-O-Fe^IV(OH)(L)₂](ClO₄)₃ (4) models (where, L = tris(3,5-dimethyl-4-methoxypyridyl-2-methyl)amine) (TPA∗)). Pronounced differences in the HERFD XAS pre-edge energies and intensities are observed for the open versus closed Fe₂O₂ cores in the model compounds. These differences are reproduced by time-dependent density functional theory (TDDFT) calculations and allow for the pre-edge energies and intensity to be directly correlated with the local active site geometric and electronic structure. A comparison of the model complex HERFD XAS data to that of MMOH_Q (the key intermediate in methane oxidation) is supportive of an open-core structure. Specifically, the large pre-edge area observed for MMOH_Q may be rationalized by invoking an open-core structure with a terminal Fe^IV=O motif, though further modulations of the core structure due to the protein environment cannot be ruled out. The present study thus motivates the need for additional experimental and theoretical studies to unambiguously assess the active site conformation of MMOH_Q.

Original language	English (US)
Pages (from-to)	18024-18033
Number of pages	10
Journal	Journal of the American Chemical Society
Volume	139
Issue number	49
DOIs	https://doi.org/10.1021/jacs.7b09560
State	Published - Dec 13 2017

Bibliographical note

Funding Information:
Former and current members of the Molecular Theory and Spectroscopy Department and Inorganic Spectroscopy Department at MPI CEC are thanked for helpful discussions regarding the computational studies and for assistance with data collection. Financial support was provided by the Max Planck Society (S.D.). J.D.L. and L.Q. acknowledge the National Institutes of Health for funding (grants GM118030 to J.D.L and GM38767 to L.Q. and postdoctoral fellowship GM113333 to C.J.A.). R.G.C. acknowledges the International Max Planck Research School on Reactive Structure Analysis for Chemical Reactions (IMPRS RECHARGE) for funding. The European Synchrotron Radiation Facility is acknowledged for providing beamtime and technical support.

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© 2017 American Chemical Society.

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10.1021/jacs.7b09560

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5729100

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@article{459f1bea9c76406693da6318f4fe5c09,

title = "High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase",

abstract = "Kα high-energy-resolution fluorescence detected X-ray absorption spectroscopy (HERFD XAS) provides a powerful tool for overcoming the limitations of conventional XAS to identify the electronic structure and coordination environment of metalloprotein active sites. Herein, Fe Kα HERFD XAS is applied to the diiron active site of soluble methane monooxygenase (sMMO) and to a series of high-valent diiron model complexes, including diamond-core [FeIV2(μ-O)2(L)2](ClO4)4] (3) and open-core [(O=FeIV-O-FeIV(OH)(L)2](ClO4)3 (4) models (where, L = tris(3,5-dimethyl-4-methoxypyridyl-2-methyl)amine) (TPA∗)). Pronounced differences in the HERFD XAS pre-edge energies and intensities are observed for the open versus closed Fe2O2 cores in the model compounds. These differences are reproduced by time-dependent density functional theory (TDDFT) calculations and allow for the pre-edge energies and intensity to be directly correlated with the local active site geometric and electronic structure. A comparison of the model complex HERFD XAS data to that of MMOHQ (the key intermediate in methane oxidation) is supportive of an open-core structure. Specifically, the large pre-edge area observed for MMOHQ may be rationalized by invoking an open-core structure with a terminal FeIV=O motif, though further modulations of the core structure due to the protein environment cannot be ruled out. The present study thus motivates the need for additional experimental and theoretical studies to unambiguously assess the active site conformation of MMOHQ.",

author = "Castillo, {Rebeca G.} and Rahul Banerjee and Allpress, {Caleb J.} and Rohde, {Gregory T.} and Eckhard Bill and Lawrence Que and Lipscomb, {John D.} and Serena DeBeer",

note = "Funding Information: Former and current members of the Molecular Theory and Spectroscopy Department and Inorganic Spectroscopy Department at MPI CEC are thanked for helpful discussions regarding the computational studies and for assistance with data collection. Financial support was provided by the Max Planck Society (S.D.). J.D.L. and L.Q. acknowledge the National Institutes of Health for funding (grants GM118030 to J.D.L and GM38767 to L.Q. and postdoctoral fellowship GM113333 to C.J.A.). R.G.C. acknowledges the International Max Planck Research School on Reactive Structure Analysis for Chemical Reactions (IMPRS RECHARGE) for funding. The European Synchrotron Radiation Facility is acknowledged for providing beamtime and technical support. Publisher Copyright: {\textcopyright} 2017 American Chemical Society.",

year = "2017",

month = dec,

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doi = "10.1021/jacs.7b09560",

language = "English (US)",

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T1 - High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

AU - Castillo, Rebeca G.

AU - Banerjee, Rahul

AU - Allpress, Caleb J.

AU - Rohde, Gregory T.

AU - Bill, Eckhard

AU - Que, Lawrence

AU - Lipscomb, John D.

AU - DeBeer, Serena

N1 - Funding Information: Former and current members of the Molecular Theory and Spectroscopy Department and Inorganic Spectroscopy Department at MPI CEC are thanked for helpful discussions regarding the computational studies and for assistance with data collection. Financial support was provided by the Max Planck Society (S.D.). J.D.L. and L.Q. acknowledge the National Institutes of Health for funding (grants GM118030 to J.D.L and GM38767 to L.Q. and postdoctoral fellowship GM113333 to C.J.A.). R.G.C. acknowledges the International Max Planck Research School on Reactive Structure Analysis for Chemical Reactions (IMPRS RECHARGE) for funding. The European Synchrotron Radiation Facility is acknowledged for providing beamtime and technical support. Publisher Copyright: © 2017 American Chemical Society.

PY - 2017/12/13

Y1 - 2017/12/13

N2 - Kα high-energy-resolution fluorescence detected X-ray absorption spectroscopy (HERFD XAS) provides a powerful tool for overcoming the limitations of conventional XAS to identify the electronic structure and coordination environment of metalloprotein active sites. Herein, Fe Kα HERFD XAS is applied to the diiron active site of soluble methane monooxygenase (sMMO) and to a series of high-valent diiron model complexes, including diamond-core [FeIV2(μ-O)2(L)2](ClO4)4] (3) and open-core [(O=FeIV-O-FeIV(OH)(L)2](ClO4)3 (4) models (where, L = tris(3,5-dimethyl-4-methoxypyridyl-2-methyl)amine) (TPA∗)). Pronounced differences in the HERFD XAS pre-edge energies and intensities are observed for the open versus closed Fe2O2 cores in the model compounds. These differences are reproduced by time-dependent density functional theory (TDDFT) calculations and allow for the pre-edge energies and intensity to be directly correlated with the local active site geometric and electronic structure. A comparison of the model complex HERFD XAS data to that of MMOHQ (the key intermediate in methane oxidation) is supportive of an open-core structure. Specifically, the large pre-edge area observed for MMOHQ may be rationalized by invoking an open-core structure with a terminal FeIV=O motif, though further modulations of the core structure due to the protein environment cannot be ruled out. The present study thus motivates the need for additional experimental and theoretical studies to unambiguously assess the active site conformation of MMOHQ.

AB - Kα high-energy-resolution fluorescence detected X-ray absorption spectroscopy (HERFD XAS) provides a powerful tool for overcoming the limitations of conventional XAS to identify the electronic structure and coordination environment of metalloprotein active sites. Herein, Fe Kα HERFD XAS is applied to the diiron active site of soluble methane monooxygenase (sMMO) and to a series of high-valent diiron model complexes, including diamond-core [FeIV2(μ-O)2(L)2](ClO4)4] (3) and open-core [(O=FeIV-O-FeIV(OH)(L)2](ClO4)3 (4) models (where, L = tris(3,5-dimethyl-4-methoxypyridyl-2-methyl)amine) (TPA∗)). Pronounced differences in the HERFD XAS pre-edge energies and intensities are observed for the open versus closed Fe2O2 cores in the model compounds. These differences are reproduced by time-dependent density functional theory (TDDFT) calculations and allow for the pre-edge energies and intensity to be directly correlated with the local active site geometric and electronic structure. A comparison of the model complex HERFD XAS data to that of MMOHQ (the key intermediate in methane oxidation) is supportive of an open-core structure. Specifically, the large pre-edge area observed for MMOHQ may be rationalized by invoking an open-core structure with a terminal FeIV=O motif, though further modulations of the core structure due to the protein environment cannot be ruled out. The present study thus motivates the need for additional experimental and theoretical studies to unambiguously assess the active site conformation of MMOHQ.

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High-Energy-Resolution Fluorescence-Detected X-ray Absorption of the Q Intermediate of Soluble Methane Monooxygenase

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