Evidence for a Di-μ-oxo diamond core in the Mn(IV)/Fe(IV) activation intermediate of ribonucleotide reductase from chlamydia trachomatis

Ryan J. Martinie, Elizabeth J. Blaesi, Carsten Krebs, Joseph M. Bollinger, Jr., Alexey Silakov, Christopher J. Pollock

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

High-valent iron and manganese complexes effect some of the most challenging biochemical reactions known, including hydrocarbon and water oxidations associated with the global carbon cycle and oxygenic photosynthesis, respectively. Their extreme reactivity presents an impediment to structural characterization, but their biological importance and potential chemical utility have, nevertheless, motivated extensive efforts toward that end. Several such intermediates accumulate during activation of class I ribonucleotide reductase (RNR) β subunits, which self-assemble dimetal cofactors with stable one-electron oxidants that serve to initiate the enzyme's free-radical mechanism. In the class I-c β subunit from Chlamydia trachomatis, a heterodinuclear Mn(II)/Fe(II) complex reacts with dioxygen to form a Mn(IV)/Fe(IV) intermediate, which undergoes reduction of the iron site to produce the active Mn(IV)/Fe(III) cofactor. Herein, we assess the structure of the Mn(IV)/Fe(IV) activation intermediate using Fe-and Mn-edge extended X-ray absorption fine structure (EXAFS) analysis and multifrequency pulse electron paramagnetic resonance (EPR) spectroscopy. The EXAFS results reveal a metal-metal vector of 2.74-2.75 Å and an intense light-atom (C/N/O) scattering interaction 1.8 Å from the Fe. Pulse EPR data reveal an exchangeable deuterium hyperfine coupling of strength |T| = 0.7 MHz, but no stronger couplings. The results suggest that the intermediate possesses a di-μ-oxo diamond core structure with a terminal hydroxide ligand to the Mn(IV).

Original languageEnglish (US)
Pages (from-to)1950-1957
Number of pages8
JournalJournal of the American Chemical Society
Volume139
Issue number5
DOIs
StatePublished - Feb 8 2017

Fingerprint

Ribonucleotide Reductases
Diamond
Chlamydia trachomatis
Electron Spin Resonance Spectroscopy
X ray absorption
Paramagnetic resonance
Diamonds
Iron
Metals
Chemical activation
X-Rays
Carbon Cycle
Photosynthesis
Deuterium
Chemical potential
Manganese
Hydrocarbons
Free radicals
Oxidants
Free Radicals

All Science Journal Classification (ASJC) codes

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

Cite this

@article{87a666267e37455fa4ae8c6e88bb72f7,
title = "Evidence for a Di-μ-oxo diamond core in the Mn(IV)/Fe(IV) activation intermediate of ribonucleotide reductase from chlamydia trachomatis",
abstract = "High-valent iron and manganese complexes effect some of the most challenging biochemical reactions known, including hydrocarbon and water oxidations associated with the global carbon cycle and oxygenic photosynthesis, respectively. Their extreme reactivity presents an impediment to structural characterization, but their biological importance and potential chemical utility have, nevertheless, motivated extensive efforts toward that end. Several such intermediates accumulate during activation of class I ribonucleotide reductase (RNR) β subunits, which self-assemble dimetal cofactors with stable one-electron oxidants that serve to initiate the enzyme's free-radical mechanism. In the class I-c β subunit from Chlamydia trachomatis, a heterodinuclear Mn(II)/Fe(II) complex reacts with dioxygen to form a Mn(IV)/Fe(IV) intermediate, which undergoes reduction of the iron site to produce the active Mn(IV)/Fe(III) cofactor. Herein, we assess the structure of the Mn(IV)/Fe(IV) activation intermediate using Fe-and Mn-edge extended X-ray absorption fine structure (EXAFS) analysis and multifrequency pulse electron paramagnetic resonance (EPR) spectroscopy. The EXAFS results reveal a metal-metal vector of 2.74-2.75 {\AA} and an intense light-atom (C/N/O) scattering interaction 1.8 {\AA} from the Fe. Pulse EPR data reveal an exchangeable deuterium hyperfine coupling of strength |T| = 0.7 MHz, but no stronger couplings. The results suggest that the intermediate possesses a di-μ-oxo diamond core structure with a terminal hydroxide ligand to the Mn(IV).",
author = "Martinie, {Ryan J.} and Blaesi, {Elizabeth J.} and Carsten Krebs and {Bollinger, Jr.}, {Joseph M.} and Alexey Silakov and Pollock, {Christopher J.}",
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Evidence for a Di-μ-oxo diamond core in the Mn(IV)/Fe(IV) activation intermediate of ribonucleotide reductase from chlamydia trachomatis. / Martinie, Ryan J.; Blaesi, Elizabeth J.; Krebs, Carsten; Bollinger, Jr., Joseph M.; Silakov, Alexey; Pollock, Christopher J.

In: Journal of the American Chemical Society, Vol. 139, No. 5, 08.02.2017, p. 1950-1957.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Evidence for a Di-μ-oxo diamond core in the Mn(IV)/Fe(IV) activation intermediate of ribonucleotide reductase from chlamydia trachomatis

AU - Martinie, Ryan J.

AU - Blaesi, Elizabeth J.

AU - Krebs, Carsten

AU - Bollinger, Jr., Joseph M.

AU - Silakov, Alexey

AU - Pollock, Christopher J.

PY - 2017/2/8

Y1 - 2017/2/8

N2 - High-valent iron and manganese complexes effect some of the most challenging biochemical reactions known, including hydrocarbon and water oxidations associated with the global carbon cycle and oxygenic photosynthesis, respectively. Their extreme reactivity presents an impediment to structural characterization, but their biological importance and potential chemical utility have, nevertheless, motivated extensive efforts toward that end. Several such intermediates accumulate during activation of class I ribonucleotide reductase (RNR) β subunits, which self-assemble dimetal cofactors with stable one-electron oxidants that serve to initiate the enzyme's free-radical mechanism. In the class I-c β subunit from Chlamydia trachomatis, a heterodinuclear Mn(II)/Fe(II) complex reacts with dioxygen to form a Mn(IV)/Fe(IV) intermediate, which undergoes reduction of the iron site to produce the active Mn(IV)/Fe(III) cofactor. Herein, we assess the structure of the Mn(IV)/Fe(IV) activation intermediate using Fe-and Mn-edge extended X-ray absorption fine structure (EXAFS) analysis and multifrequency pulse electron paramagnetic resonance (EPR) spectroscopy. The EXAFS results reveal a metal-metal vector of 2.74-2.75 Å and an intense light-atom (C/N/O) scattering interaction 1.8 Å from the Fe. Pulse EPR data reveal an exchangeable deuterium hyperfine coupling of strength |T| = 0.7 MHz, but no stronger couplings. The results suggest that the intermediate possesses a di-μ-oxo diamond core structure with a terminal hydroxide ligand to the Mn(IV).

AB - High-valent iron and manganese complexes effect some of the most challenging biochemical reactions known, including hydrocarbon and water oxidations associated with the global carbon cycle and oxygenic photosynthesis, respectively. Their extreme reactivity presents an impediment to structural characterization, but their biological importance and potential chemical utility have, nevertheless, motivated extensive efforts toward that end. Several such intermediates accumulate during activation of class I ribonucleotide reductase (RNR) β subunits, which self-assemble dimetal cofactors with stable one-electron oxidants that serve to initiate the enzyme's free-radical mechanism. In the class I-c β subunit from Chlamydia trachomatis, a heterodinuclear Mn(II)/Fe(II) complex reacts with dioxygen to form a Mn(IV)/Fe(IV) intermediate, which undergoes reduction of the iron site to produce the active Mn(IV)/Fe(III) cofactor. Herein, we assess the structure of the Mn(IV)/Fe(IV) activation intermediate using Fe-and Mn-edge extended X-ray absorption fine structure (EXAFS) analysis and multifrequency pulse electron paramagnetic resonance (EPR) spectroscopy. The EXAFS results reveal a metal-metal vector of 2.74-2.75 Å and an intense light-atom (C/N/O) scattering interaction 1.8 Å from the Fe. Pulse EPR data reveal an exchangeable deuterium hyperfine coupling of strength |T| = 0.7 MHz, but no stronger couplings. The results suggest that the intermediate possesses a di-μ-oxo diamond core structure with a terminal hydroxide ligand to the Mn(IV).

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