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

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

doi:10.1021/jacs.6b07227

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

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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 in this paper, 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.

Authors:

Sutherlin, Kyle D. ^[1]; Liu, Lei V. ^[1]; Lee, Yong-Min ^[2]; Kwak, Yeonju ^[1]; Yoda, Yoshitaka ^[3]; Saito, Makina ^[4]; Kurokuzu, Masayuki ^[4]; Kobayashi, Yasuhiro ^[4]; Seto, Makoto ^[4]; Que, Lawrence ^[5]; Nam, Wonwoo ^[2]; Solomon, Edward I. ^[6]

Stanford Univ., CA (United States). Dept. of Chemistry
Ewha Womans Univ., Seoul (Korea). Center for Biomimetic Systems, Dept. of Bioinspired Science, Dept. of Chemistry and Nano Science
Japan Synchrotron Radiation Research Inst. (JASRI), Hyogo (Japan). SPring-8
Kyoto Univ., Osaka (Japan). Research Reactor Inst.
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Chemistry
Stanford Univ., CA (United States). Dept. of Chemistry; SLAC National Accelerator Lab., Menlo Park, CA (United States)

Publication Date:: 2016-11-02

Research Org.:: SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE; National Institutes of Health (NIH); National Research Foundation of Korea (NRF); Japan Society for the Promotion of Science (JSPS); National Science Foundation (NSF)

OSTI Identifier:: 1360201

Grant/Contract Number:: AC02-76SF00515; CHE-1361773; NRF-2010-00353; NRF-2012R1A3A2048842; 24221005; GM-40392

Resource Type:: Accepted Manuscript

Journal Name:: Journal of the American Chemical Society

Additional Journal Information:: Journal Volume: 138; Journal Issue: 43; Journal ID: ISSN 0002-7863

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY

Citation Formats


                    Sutherlin, Kyle D., Liu, Lei V., Lee, Yong-Min, Kwak, Yeonju, Yoda, Yoshitaka, Saito, Makina, Kurokuzu, Masayuki, Kobayashi, Yasuhiro, Seto, Makoto, Que, Lawrence, Nam, Wonwoo, and Solomon, Edward I. Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites.  United States: N. p., 2016. 
Web.  doi:10.1021/jacs.6b07227.

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                    Sutherlin, Kyle D., Liu, Lei V., Lee, Yong-Min, Kwak, Yeonju, Yoda, Yoshitaka, Saito, Makina, Kurokuzu, Masayuki, Kobayashi, Yasuhiro, Seto, Makoto, Que, Lawrence, Nam, Wonwoo, & Solomon, Edward I. Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites.  United States.  https://doi.org/10.1021/jacs.6b07227

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                    Sutherlin, Kyle D., Liu, Lei V., Lee, Yong-Min, Kwak, Yeonju, Yoda, Yoshitaka, Saito, Makina, Kurokuzu, Masayuki, Kobayashi, Yasuhiro, Seto, Makoto, Que, Lawrence, Nam, Wonwoo, and Solomon, Edward I. Wed .  
"Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites".  United States.  https://doi.org/10.1021/jacs.6b07227.  https://www.osti.gov/servlets/purl/1360201.

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@article{osti_1360201,

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

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

  abstractNote = {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 in this paper, 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.},

  doi          = {10.1021/jacs.6b07227},

  journal      = {Journal of the American Chemical Society},

  number       = 43,

  volume       = 138,

  place        = {United States},

  year         = {2016},

  month        = {11}

}

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