Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites

Kyle D. Sutherlin; Lei V. Liu; Yong Min Lee; Yeonju Kwak; Yoshitaka Yoda; Makina Saito; Masayuki Kurokuzu; Yasuhiro Kobayashi; Makoto Seto; Lawrence Que; Wonwoo Nam; Edward I. Solomon

doi:10.1021/jacs.6b07227

Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites

Kyle D. Sutherlin, Lei V. Liu, Yong Min Lee, Yeonju Kwak, Yoshitaka Yoda, Makina Saito, Masayuki Kurokuzu, Yasuhiro Kobayashi, Makoto Seto, Lawrence Que, Wonwoo Nam, Edward I. Solomon

Chemistry & Nanoscience

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

6 Scopus citations

Abstract

Fe^III-(hydro)peroxy intermediates have been isolated in two classes of mononuclear nonheme Fe enzymes that are important in bioremediation: the Rieske dioxygenases and the extradiol dioxygenases. The binding mode and protonation state of the peroxide moieties in these intermediates are not well-defined, due to a lack of vibrational structural data. Nuclear resonance vibrational spectroscopy (NRVS) is an important technique for obtaining vibrational information on these and other intermediates, as it is sensitive to all normal modes with Fe displacement. Here, we present the NRVS spectra of side-on Fe^III-peroxy and end-on Fe^III-hydroperoxy model complexes and assign these spectra using calibrated DFT calculations. We then use DFT calculations to define and understand the changes in the NRVS spectra that arise from protonation and from opening the Fe-O-O angle. This study identifies four spectroscopic handles that will enable definition of the binding mode and protonation state of Fe^III-peroxy intermediates in mononuclear nonheme Fe enzymes. These structural differences are important in determining the frontier molecular orbitals available for reactivity.

Original language	English
Pages (from-to)	14294-14302
Number of pages	9
Journal	Journal of the American Chemical Society
Volume	138
Issue number	43
DOIs	https://doi.org/10.1021/jacs.6b07227
State	Published - 2 Nov 2016

Bibliographical note

Funding Information:
Funding for this work was provided by the National Institutes of Health (GM-40392 to E.I.S.), the NRF of Korea through CRI (NRF-2012R1A3A2048842 to W.N.) and GRL (NRF-2010-00353 to W.N.), JSPS KAKENHI (Grant No. 24221005 to M. Seto), and the U.S. National Science Foundation (CHE-1361773 to L.Q.). Synchrotron experiments at SPring-8 were performed with the approval of the Japan Synchrotron Radiation Research Institute (JASRI; Proposal No. 2013B0105).

Publisher Copyright:
© 2016 American Chemical Society.

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10.1021/jacs.6b07227

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@article{e93b9ef73f414e8285e96290cc882ddf,

title = "Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites",

abstract = "FeIII-(hydro)peroxy intermediates have been isolated in two classes of mononuclear nonheme Fe enzymes that are important in bioremediation: the Rieske dioxygenases and the extradiol dioxygenases. The binding mode and protonation state of the peroxide moieties in these intermediates are not well-defined, due to a lack of vibrational structural data. Nuclear resonance vibrational spectroscopy (NRVS) is an important technique for obtaining vibrational information on these and other intermediates, as it is sensitive to all normal modes with Fe displacement. Here, we present the NRVS spectra of side-on FeIII-peroxy and end-on FeIII-hydroperoxy model complexes and assign these spectra using calibrated DFT calculations. We then use DFT calculations to define and understand the changes in the NRVS spectra that arise from protonation and from opening the Fe-O-O angle. This study identifies four spectroscopic handles that will enable definition of the binding mode and protonation state of FeIII-peroxy intermediates in mononuclear nonheme Fe enzymes. These structural differences are important in determining the frontier molecular orbitals available for reactivity.",

author = "Sutherlin, {Kyle D.} and Liu, {Lei V.} and Lee, {Yong Min} and Yeonju Kwak and Yoshitaka Yoda and Makina Saito and Masayuki Kurokuzu and Yasuhiro Kobayashi and Makoto Seto and Lawrence Que and Wonwoo Nam and Solomon, {Edward I.}",

note = "Funding Information: Funding for this work was provided by the National Institutes of Health (GM-40392 to E.I.S.), the NRF of Korea through CRI (NRF-2012R1A3A2048842 to W.N.) and GRL (NRF-2010-00353 to W.N.), JSPS KAKENHI (Grant No. 24221005 to M. Seto), and the U.S. National Science Foundation (CHE-1361773 to L.Q.). Synchrotron experiments at SPring-8 were performed with the approval of the Japan Synchrotron Radiation Research Institute (JASRI; Proposal No. 2013B0105). Publisher Copyright: {\textcopyright} 2016 American Chemical Society.",

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language = "English",

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T1 - Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites

AU - Sutherlin, Kyle D.

AU - Liu, Lei V.

AU - Lee, Yong Min

AU - Kwak, Yeonju

AU - Yoda, Yoshitaka

AU - Saito, Makina

AU - Kurokuzu, Masayuki

AU - Kobayashi, Yasuhiro

AU - Seto, Makoto

AU - Que, Lawrence

AU - Nam, Wonwoo

AU - Solomon, Edward I.

N1 - Funding Information: Funding for this work was provided by the National Institutes of Health (GM-40392 to E.I.S.), the NRF of Korea through CRI (NRF-2012R1A3A2048842 to W.N.) and GRL (NRF-2010-00353 to W.N.), JSPS KAKENHI (Grant No. 24221005 to M. Seto), and the U.S. National Science Foundation (CHE-1361773 to L.Q.). Synchrotron experiments at SPring-8 were performed with the approval of the Japan Synchrotron Radiation Research Institute (JASRI; Proposal No. 2013B0105). Publisher Copyright: © 2016 American Chemical Society.

PY - 2016/11/2

Y1 - 2016/11/2

N2 - FeIII-(hydro)peroxy intermediates have been isolated in two classes of mononuclear nonheme Fe enzymes that are important in bioremediation: the Rieske dioxygenases and the extradiol dioxygenases. The binding mode and protonation state of the peroxide moieties in these intermediates are not well-defined, due to a lack of vibrational structural data. Nuclear resonance vibrational spectroscopy (NRVS) is an important technique for obtaining vibrational information on these and other intermediates, as it is sensitive to all normal modes with Fe displacement. Here, we present the NRVS spectra of side-on FeIII-peroxy and end-on FeIII-hydroperoxy model complexes and assign these spectra using calibrated DFT calculations. We then use DFT calculations to define and understand the changes in the NRVS spectra that arise from protonation and from opening the Fe-O-O angle. This study identifies four spectroscopic handles that will enable definition of the binding mode and protonation state of FeIII-peroxy intermediates in mononuclear nonheme Fe enzymes. These structural differences are important in determining the frontier molecular orbitals available for reactivity.

AB - FeIII-(hydro)peroxy intermediates have been isolated in two classes of mononuclear nonheme Fe enzymes that are important in bioremediation: the Rieske dioxygenases and the extradiol dioxygenases. The binding mode and protonation state of the peroxide moieties in these intermediates are not well-defined, due to a lack of vibrational structural data. Nuclear resonance vibrational spectroscopy (NRVS) is an important technique for obtaining vibrational information on these and other intermediates, as it is sensitive to all normal modes with Fe displacement. Here, we present the NRVS spectra of side-on FeIII-peroxy and end-on FeIII-hydroperoxy model complexes and assign these spectra using calibrated DFT calculations. We then use DFT calculations to define and understand the changes in the NRVS spectra that arise from protonation and from opening the Fe-O-O angle. This study identifies four spectroscopic handles that will enable definition of the binding mode and protonation state of FeIII-peroxy intermediates in mononuclear nonheme Fe enzymes. These structural differences are important in determining the frontier molecular orbitals available for reactivity.

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JO - Journal of the American Chemical Society

JF - Journal of the American Chemical Society

IS - 43

ER -

Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites

Abstract

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