Electronic Structure of the Ferryl Intermediate in the α-Ketoglutarate Dependent Non-Heme Iron Halogenase SyrB2: Contributions to H Atom Abstraction Reactivity

Martin Srnec, Shaun D. Wong, Megan L. Matthews, Carsten Krebs, Joseph M. Bollinger, Jr., Edward I. Solomon

Research output: Contribution to journalArticle

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Abstract

Low temperature magnetic circular dichroism (LT MCD) spectroscopy in combination with quantum-chemical calculations are used to define the electronic structure associated with the geometric structure of the FeIV=O intermediate in SyrB2 that was previously determined by nuclear resonance vibrational spectroscopy. These studies elucidate key frontier molecular orbitals (FMOs) and their contribution to H atom abstraction reactivity. The VT MCD spectra of the enzymatic S = 2 FeIV=O intermediate with Br- ligation contain information-rich features that largely parallel the corresponding spectra of the S = 2 model complex (TMG3tren)FeIV=O (Srnec, M.; Wong, S. D.; England, J; Que, L; Solomon, E. I. Proc. Natl. Acad. Sci. USA 2012, 109, 14326-14331). However, quantitative differences are observed that correlate with π-anisotropy and oxo donor strength that perturb FMOs and affect reactivity. Due to π-anisotropy, the FeIV=O active site exhibits enhanced reactivity in the direction of the substrate cavity that proceeds through a π-channel that is controlled by perpendicular orientation of the substrate C-H bond relative to the halide-FeIV=O plane. Also, the increased intrinsic reactivity of the SyrB2 intermediate relative to the ferryl model complex is correlated to a higher oxyl character of the FeIV=O at the transition states resulting from the weaker ligand field of the halogenase.

Original languageEnglish (US)
Pages (from-to)5110-5122
Number of pages13
JournalJournal of the American Chemical Society
Volume138
Issue number15
DOIs
StatePublished - May 4 2016

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Anisotropy
Molecular orbitals
Electronic structure
Spectrum Analysis
Iron
Circular dichroism spectroscopy
Vibrational spectroscopy
Atoms
Substrates
Circular Dichroism
England
Ligation
Catalytic Domain
Ligands
Temperature
Direction compound
S(2) complex

All Science Journal Classification (ASJC) codes

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

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title = "Electronic Structure of the Ferryl Intermediate in the α-Ketoglutarate Dependent Non-Heme Iron Halogenase SyrB2: Contributions to H Atom Abstraction Reactivity",
abstract = "Low temperature magnetic circular dichroism (LT MCD) spectroscopy in combination with quantum-chemical calculations are used to define the electronic structure associated with the geometric structure of the FeIV=O intermediate in SyrB2 that was previously determined by nuclear resonance vibrational spectroscopy. These studies elucidate key frontier molecular orbitals (FMOs) and their contribution to H atom abstraction reactivity. The VT MCD spectra of the enzymatic S = 2 FeIV=O intermediate with Br- ligation contain information-rich features that largely parallel the corresponding spectra of the S = 2 model complex (TMG3tren)FeIV=O (Srnec, M.; Wong, S. D.; England, J; Que, L; Solomon, E. I. Proc. Natl. Acad. Sci. USA 2012, 109, 14326-14331). However, quantitative differences are observed that correlate with π-anisotropy and oxo donor strength that perturb FMOs and affect reactivity. Due to π-anisotropy, the FeIV=O active site exhibits enhanced reactivity in the direction of the substrate cavity that proceeds through a π-channel that is controlled by perpendicular orientation of the substrate C-H bond relative to the halide-FeIV=O plane. Also, the increased intrinsic reactivity of the SyrB2 intermediate relative to the ferryl model complex is correlated to a higher oxyl character of the FeIV=O at the transition states resulting from the weaker ligand field of the halogenase.",
author = "Martin Srnec and Wong, {Shaun D.} and Matthews, {Megan L.} and Carsten Krebs and {Bollinger, Jr.}, {Joseph M.} and Solomon, {Edward I.}",
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Electronic Structure of the Ferryl Intermediate in the α-Ketoglutarate Dependent Non-Heme Iron Halogenase SyrB2 : Contributions to H Atom Abstraction Reactivity. / Srnec, Martin; Wong, Shaun D.; Matthews, Megan L.; Krebs, Carsten; Bollinger, Jr., Joseph M.; Solomon, Edward I.

In: Journal of the American Chemical Society, Vol. 138, No. 15, 04.05.2016, p. 5110-5122.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Electronic Structure of the Ferryl Intermediate in the α-Ketoglutarate Dependent Non-Heme Iron Halogenase SyrB2

T2 - Contributions to H Atom Abstraction Reactivity

AU - Srnec, Martin

AU - Wong, Shaun D.

AU - Matthews, Megan L.

AU - Krebs, Carsten

AU - Bollinger, Jr., Joseph M.

AU - Solomon, Edward I.

PY - 2016/5/4

Y1 - 2016/5/4

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