Characterization of the bridged hyponitrite complex {[Fe(OEP)] 2(μ-N2O2)}

Reactivity of hyponitrite complexes and biological relevance

Timothy C. Berto, Nan Xu, Se Ryeon Lee, Anne J. McNeil, E. Ercan Alp, Jiyong Zhao, George B. Richter-Addo, Nicolai Lehnert

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

The detoxification of nitric oxide (NO) by bacterial NO reductase (NorBC) represents a paradigm of how NO can be detoxified anaerobically in cells. In order to elucidate the mechanism of this enzyme, model complexes provide a convenient means to assess potential reaction intermediates. In particular, there have been many proposed mechanisms that invoke the formation of a hyponitrite bridge between the heme b3 and nonheme iron (Fe B) centers within the NorBC active site. However, the reactivity of bridged iron hyponitrite complexes has not been investigated much in the literature. The model complex {[Fe(OEP)]2(μ-N2O 2)} offers a unique opportunity to study the electronic structure and reactivity of such a hyponitrite-bridged complex. Here we report the detailed characterization of {[Fe(OEP)]2(μ-N2O2)} using a combination of IR, nuclear resonance vibrational spectroscopy, electron paramagnetic resonance, and magnetic circular dichroism spectroscopy along with SQUID magnetometry. These results show that the ground-state electronic structure of this complex is best described as having two intermediate-spin (S = 3/2) iron centers that are weakly antiferromagnetically coupled across the N2O2 2- bridge. The analogous complex {[Fe(PPDME)]2(μ-N2O2)} shows overall similar properties. Finally, we report the unexpected reaction of {[Fe(OEP)]2(μ-N2O2)} in the presence and absence of 1-methylimidizole to yield [Fe(OEP)(NO)]. Density functional theory calculations are used to rationalize why {[Fe(OEP)]2(μ-N 2O2)} cannot be formed directly by dimerization of [Fe(OEP)(NO)] and why only the reverse reaction is observed experimentally. These results thus provide insight into the general reactivity of hyponitrite-bridged iron complexes with general relevance for the N-N bond-forming step in NorBC.

Original languageEnglish (US)
Pages (from-to)6398-6414
Number of pages17
JournalInorganic Chemistry
Volume53
Issue number13
DOIs
StatePublished - Jul 7 2014

Fingerprint

nitric oxide
Nitric Oxide
Iron
reactivity
iron
Electronic structure
Circular dichroism spectroscopy
Reaction intermediates
Vibrational spectroscopy
Detoxification
Dimerization
SQUIDs
electronic structure
Heme
reaction intermediates
Ground state
Density functional theory
Paramagnetic resonance
dimerization
spectroscopy

All Science Journal Classification (ASJC) codes

  • Physical and Theoretical Chemistry
  • Inorganic Chemistry

Cite this

Berto, Timothy C. ; Xu, Nan ; Lee, Se Ryeon ; McNeil, Anne J. ; Alp, E. Ercan ; Zhao, Jiyong ; Richter-Addo, George B. ; Lehnert, Nicolai. / Characterization of the bridged hyponitrite complex {[Fe(OEP)] 2(μ-N2O2)} : Reactivity of hyponitrite complexes and biological relevance. In: Inorganic Chemistry. 2014 ; Vol. 53, No. 13. pp. 6398-6414.
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abstract = "The detoxification of nitric oxide (NO) by bacterial NO reductase (NorBC) represents a paradigm of how NO can be detoxified anaerobically in cells. In order to elucidate the mechanism of this enzyme, model complexes provide a convenient means to assess potential reaction intermediates. In particular, there have been many proposed mechanisms that invoke the formation of a hyponitrite bridge between the heme b3 and nonheme iron (Fe B) centers within the NorBC active site. However, the reactivity of bridged iron hyponitrite complexes has not been investigated much in the literature. The model complex {[Fe(OEP)]2(μ-N2O 2)} offers a unique opportunity to study the electronic structure and reactivity of such a hyponitrite-bridged complex. Here we report the detailed characterization of {[Fe(OEP)]2(μ-N2O2)} using a combination of IR, nuclear resonance vibrational spectroscopy, electron paramagnetic resonance, and magnetic circular dichroism spectroscopy along with SQUID magnetometry. These results show that the ground-state electronic structure of this complex is best described as having two intermediate-spin (S = 3/2) iron centers that are weakly antiferromagnetically coupled across the N2O2 2- bridge. The analogous complex {[Fe(PPDME)]2(μ-N2O2)} shows overall similar properties. Finally, we report the unexpected reaction of {[Fe(OEP)]2(μ-N2O2)} in the presence and absence of 1-methylimidizole to yield [Fe(OEP)(NO)]. Density functional theory calculations are used to rationalize why {[Fe(OEP)]2(μ-N 2O2)} cannot be formed directly by dimerization of [Fe(OEP)(NO)] and why only the reverse reaction is observed experimentally. These results thus provide insight into the general reactivity of hyponitrite-bridged iron complexes with general relevance for the N-N bond-forming step in NorBC.",
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Characterization of the bridged hyponitrite complex {[Fe(OEP)] 2(μ-N2O2)} : Reactivity of hyponitrite complexes and biological relevance. / Berto, Timothy C.; Xu, Nan; Lee, Se Ryeon; McNeil, Anne J.; Alp, E. Ercan; Zhao, Jiyong; Richter-Addo, George B.; Lehnert, Nicolai.

In: Inorganic Chemistry, Vol. 53, No. 13, 07.07.2014, p. 6398-6414.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Characterization of the bridged hyponitrite complex {[Fe(OEP)] 2(μ-N2O2)}

T2 - Reactivity of hyponitrite complexes and biological relevance

AU - Berto, Timothy C.

AU - Xu, Nan

AU - Lee, Se Ryeon

AU - McNeil, Anne J.

AU - Alp, E. Ercan

AU - Zhao, Jiyong

AU - Richter-Addo, George B.

AU - Lehnert, Nicolai

PY - 2014/7/7

Y1 - 2014/7/7

N2 - The detoxification of nitric oxide (NO) by bacterial NO reductase (NorBC) represents a paradigm of how NO can be detoxified anaerobically in cells. In order to elucidate the mechanism of this enzyme, model complexes provide a convenient means to assess potential reaction intermediates. In particular, there have been many proposed mechanisms that invoke the formation of a hyponitrite bridge between the heme b3 and nonheme iron (Fe B) centers within the NorBC active site. However, the reactivity of bridged iron hyponitrite complexes has not been investigated much in the literature. The model complex {[Fe(OEP)]2(μ-N2O 2)} offers a unique opportunity to study the electronic structure and reactivity of such a hyponitrite-bridged complex. Here we report the detailed characterization of {[Fe(OEP)]2(μ-N2O2)} using a combination of IR, nuclear resonance vibrational spectroscopy, electron paramagnetic resonance, and magnetic circular dichroism spectroscopy along with SQUID magnetometry. These results show that the ground-state electronic structure of this complex is best described as having two intermediate-spin (S = 3/2) iron centers that are weakly antiferromagnetically coupled across the N2O2 2- bridge. The analogous complex {[Fe(PPDME)]2(μ-N2O2)} shows overall similar properties. Finally, we report the unexpected reaction of {[Fe(OEP)]2(μ-N2O2)} in the presence and absence of 1-methylimidizole to yield [Fe(OEP)(NO)]. Density functional theory calculations are used to rationalize why {[Fe(OEP)]2(μ-N 2O2)} cannot be formed directly by dimerization of [Fe(OEP)(NO)] and why only the reverse reaction is observed experimentally. These results thus provide insight into the general reactivity of hyponitrite-bridged iron complexes with general relevance for the N-N bond-forming step in NorBC.

AB - The detoxification of nitric oxide (NO) by bacterial NO reductase (NorBC) represents a paradigm of how NO can be detoxified anaerobically in cells. In order to elucidate the mechanism of this enzyme, model complexes provide a convenient means to assess potential reaction intermediates. In particular, there have been many proposed mechanisms that invoke the formation of a hyponitrite bridge between the heme b3 and nonheme iron (Fe B) centers within the NorBC active site. However, the reactivity of bridged iron hyponitrite complexes has not been investigated much in the literature. The model complex {[Fe(OEP)]2(μ-N2O 2)} offers a unique opportunity to study the electronic structure and reactivity of such a hyponitrite-bridged complex. Here we report the detailed characterization of {[Fe(OEP)]2(μ-N2O2)} using a combination of IR, nuclear resonance vibrational spectroscopy, electron paramagnetic resonance, and magnetic circular dichroism spectroscopy along with SQUID magnetometry. These results show that the ground-state electronic structure of this complex is best described as having two intermediate-spin (S = 3/2) iron centers that are weakly antiferromagnetically coupled across the N2O2 2- bridge. The analogous complex {[Fe(PPDME)]2(μ-N2O2)} shows overall similar properties. Finally, we report the unexpected reaction of {[Fe(OEP)]2(μ-N2O2)} in the presence and absence of 1-methylimidizole to yield [Fe(OEP)(NO)]. Density functional theory calculations are used to rationalize why {[Fe(OEP)]2(μ-N 2O2)} cannot be formed directly by dimerization of [Fe(OEP)(NO)] and why only the reverse reaction is observed experimentally. These results thus provide insight into the general reactivity of hyponitrite-bridged iron complexes with general relevance for the N-N bond-forming step in NorBC.

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