Unusual Synthetic Pathway for an {Fe(NO)2}9 Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy

Amy L. Speelman; Bo Zhang; Alexey Silakov; Kelsey M. Skodje; E. Ercan Alp; Jiyong Zhao; Michael Y. Hu; Eunsuk Kim; Carsten Krebs; Nicolai Lehnert

doi:10.1021/acs.inorgchem.6b00510

Unusual Synthetic Pathway for an {Fe(NO)₂}⁹ Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy

Amy L. Speelman
, Bo Zhang
, Alexey Silakov
, Kelsey M. Skodje
, E. Ercan Alp
, Jiyong Zhao
, Michael Y. Hu
, Eunsuk Kim
, Carsten Krebs
, Nicolai Lehnert

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

64 Scopus citations

Abstract

Dinitrosyl iron complexes (DNICs) are among the most abundant NO-derived cellular species. Monomeric DNICs can exist in the {Fe(NO)₂}⁹ or {Fe(NO)₂}¹⁰ oxidation state (in the Enemark-Feltham notation). However, experimental studies of analogous DNICs in both oxidation states are rare, which prevents a thorough understanding of the differences in the electronic structures of these species. Here, the {Fe(NO)₂}⁹ DNIC [Fe(dmp)(NO)₂](OTf) (1; dmp = 2,9-dimethyl-1,10-phenanthroline) is synthesized from a ferrous precursor via an unusual pathway, involving disproportionation of an {FeNO}⁷ complex to yield the {Fe(NO)₂}⁹ DNIC and a ferric species, which is subsequently reduced by NO gas to generate a ferrous complex that re-enters the reaction cycle. In contrast to most {Fe(NO)₂}⁹ DNICs with neutral N-donor ligands, 1 exhibits high solution stability and can be characterized structurally and spectroscopically. Reduction of 1 yields the corresponding {Fe(NO)₂}¹⁰ DNIC [Fe(dmp)(NO)₂] (2). The Mössbauer isomer shift of 2 is 0.08 mm/s smaller than that of 1, which indicates that the iron center is slightly more oxidized in the reduced complex. The nuclear resonance vibrational spectra (NRVS) of 1 and 2 are distinct and provide direct experimental insight into differences in bonding in these complexes. In particular, the symmetric out-of-plane Fe-N-O bending mode is shifted to higher energy by 188 cm^-1 in 2 in comparison to 1. Using quantum chemistry centered normal coordinate analysis (QCC-NCA), this is shown to arise from an increase in Fe-NO bond order and a stiffening of the Fe(NO)₂ unit upon reduction of 1 to 2. DFT calculations demonstrate that the changes in bonding arise from an iron-centered reduction which leads to a distinct increase in Fe-NO π-back-bonding in {Fe(NO)₂}¹⁰ DNICs in comparison to the corresponding {Fe(NO)₂}⁹ complexes, in agreement with all experimental findings. Finally, the implications of the electronic structure of DNICs for their reactivity are discussed, especially with respect to N-N bond formation in NO reductases.

Original language	English (US)
Pages (from-to)	5485-5501
Number of pages	17
Journal	Inorganic chemistry
Volume	55
Issue number	11
DOIs	https://doi.org/10.1021/acs.inorgchem.6b00510
State	Published - Jun 6 2016

All Science Journal Classification (ASJC) codes

Physical and Theoretical Chemistry
Inorganic Chemistry

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10.1021/acs.inorgchem.6b00510

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Speelman, A. L., Zhang, B., Silakov, A., Skodje, K. M., Alp, E. E., Zhao, J., Hu, M. Y., Kim, E., Krebs, C., & Lehnert, N. (2016). Unusual Synthetic Pathway for an {Fe(NO)₂}⁹ Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy. Inorganic chemistry, 55(11), 5485-5501. https://doi.org/10.1021/acs.inorgchem.6b00510

@article{00a5bb3be26e4732bc37e3ca2e57276d,

title = "Unusual Synthetic Pathway for an \{Fe(NO)2\}9 Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy",

abstract = "Dinitrosyl iron complexes (DNICs) are among the most abundant NO-derived cellular species. Monomeric DNICs can exist in the \{Fe(NO)2\}9 or \{Fe(NO)2\}10 oxidation state (in the Enemark-Feltham notation). However, experimental studies of analogous DNICs in both oxidation states are rare, which prevents a thorough understanding of the differences in the electronic structures of these species. Here, the \{Fe(NO)2\}9 DNIC [Fe(dmp)(NO)2](OTf) (1; dmp = 2,9-dimethyl-1,10-phenanthroline) is synthesized from a ferrous precursor via an unusual pathway, involving disproportionation of an \{FeNO\}7 complex to yield the \{Fe(NO)2\}9 DNIC and a ferric species, which is subsequently reduced by NO gas to generate a ferrous complex that re-enters the reaction cycle. In contrast to most \{Fe(NO)2\}9 DNICs with neutral N-donor ligands, 1 exhibits high solution stability and can be characterized structurally and spectroscopically. Reduction of 1 yields the corresponding \{Fe(NO)2\}10 DNIC [Fe(dmp)(NO)2] (2). The M{\"o}ssbauer isomer shift of 2 is 0.08 mm/s smaller than that of 1, which indicates that the iron center is slightly more oxidized in the reduced complex. The nuclear resonance vibrational spectra (NRVS) of 1 and 2 are distinct and provide direct experimental insight into differences in bonding in these complexes. In particular, the symmetric out-of-plane Fe-N-O bending mode is shifted to higher energy by 188 cm-1 in 2 in comparison to 1. Using quantum chemistry centered normal coordinate analysis (QCC-NCA), this is shown to arise from an increase in Fe-NO bond order and a stiffening of the Fe(NO)2 unit upon reduction of 1 to 2. DFT calculations demonstrate that the changes in bonding arise from an iron-centered reduction which leads to a distinct increase in Fe-NO π-back-bonding in \{Fe(NO)2\}10 DNICs in comparison to the corresponding \{Fe(NO)2\}9 complexes, in agreement with all experimental findings. Finally, the implications of the electronic structure of DNICs for their reactivity are discussed, especially with respect to N-N bond formation in NO reductases.",

author = "Speelman, \{Amy L.\} and Bo Zhang and Alexey Silakov and Skodje, \{Kelsey M.\} and Alp, \{E. Ercan\} and Jiyong Zhao and Hu, \{Michael Y.\} and Eunsuk Kim and Carsten Krebs and Nicolai Lehnert",

note = "Publisher Copyright: {\textcopyright} 2016 American Chemical Society.",

year = "2016",

month = jun,

day = "6",

doi = "10.1021/acs.inorgchem.6b00510",

language = "English (US)",

volume = "55",

pages = "5485--5501",

journal = "Inorganic chemistry",

issn = "0020-1669",

publisher = "American Chemical Society",

number = "11",

}

Speelman, AL, Zhang, B, Silakov, A, Skodje, KM, Alp, EE, Zhao, J, Hu, MY, Kim, E, Krebs, C & Lehnert, N 2016, 'Unusual Synthetic Pathway for an {Fe(NO)₂}⁹ Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy', Inorganic chemistry, vol. 55, no. 11, pp. 5485-5501. https://doi.org/10.1021/acs.inorgchem.6b00510

TY - JOUR

T1 - Unusual Synthetic Pathway for an {Fe(NO)2}9 Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy

AU - Speelman, Amy L.

AU - Zhang, Bo

AU - Silakov, Alexey

AU - Skodje, Kelsey M.

AU - Alp, E. Ercan

AU - Zhao, Jiyong

AU - Hu, Michael Y.

AU - Kim, Eunsuk

AU - Krebs, Carsten

AU - Lehnert, Nicolai

PY - 2016/6/6

Y1 - 2016/6/6

N2 - Dinitrosyl iron complexes (DNICs) are among the most abundant NO-derived cellular species. Monomeric DNICs can exist in the {Fe(NO)2}9 or {Fe(NO)2}10 oxidation state (in the Enemark-Feltham notation). However, experimental studies of analogous DNICs in both oxidation states are rare, which prevents a thorough understanding of the differences in the electronic structures of these species. Here, the {Fe(NO)2}9 DNIC [Fe(dmp)(NO)2](OTf) (1; dmp = 2,9-dimethyl-1,10-phenanthroline) is synthesized from a ferrous precursor via an unusual pathway, involving disproportionation of an {FeNO}7 complex to yield the {Fe(NO)2}9 DNIC and a ferric species, which is subsequently reduced by NO gas to generate a ferrous complex that re-enters the reaction cycle. In contrast to most {Fe(NO)2}9 DNICs with neutral N-donor ligands, 1 exhibits high solution stability and can be characterized structurally and spectroscopically. Reduction of 1 yields the corresponding {Fe(NO)2}10 DNIC [Fe(dmp)(NO)2] (2). The Mössbauer isomer shift of 2 is 0.08 mm/s smaller than that of 1, which indicates that the iron center is slightly more oxidized in the reduced complex. The nuclear resonance vibrational spectra (NRVS) of 1 and 2 are distinct and provide direct experimental insight into differences in bonding in these complexes. In particular, the symmetric out-of-plane Fe-N-O bending mode is shifted to higher energy by 188 cm-1 in 2 in comparison to 1. Using quantum chemistry centered normal coordinate analysis (QCC-NCA), this is shown to arise from an increase in Fe-NO bond order and a stiffening of the Fe(NO)2 unit upon reduction of 1 to 2. DFT calculations demonstrate that the changes in bonding arise from an iron-centered reduction which leads to a distinct increase in Fe-NO π-back-bonding in {Fe(NO)2}10 DNICs in comparison to the corresponding {Fe(NO)2}9 complexes, in agreement with all experimental findings. Finally, the implications of the electronic structure of DNICs for their reactivity are discussed, especially with respect to N-N bond formation in NO reductases.

AB - Dinitrosyl iron complexes (DNICs) are among the most abundant NO-derived cellular species. Monomeric DNICs can exist in the {Fe(NO)2}9 or {Fe(NO)2}10 oxidation state (in the Enemark-Feltham notation). However, experimental studies of analogous DNICs in both oxidation states are rare, which prevents a thorough understanding of the differences in the electronic structures of these species. Here, the {Fe(NO)2}9 DNIC [Fe(dmp)(NO)2](OTf) (1; dmp = 2,9-dimethyl-1,10-phenanthroline) is synthesized from a ferrous precursor via an unusual pathway, involving disproportionation of an {FeNO}7 complex to yield the {Fe(NO)2}9 DNIC and a ferric species, which is subsequently reduced by NO gas to generate a ferrous complex that re-enters the reaction cycle. In contrast to most {Fe(NO)2}9 DNICs with neutral N-donor ligands, 1 exhibits high solution stability and can be characterized structurally and spectroscopically. Reduction of 1 yields the corresponding {Fe(NO)2}10 DNIC [Fe(dmp)(NO)2] (2). The Mössbauer isomer shift of 2 is 0.08 mm/s smaller than that of 1, which indicates that the iron center is slightly more oxidized in the reduced complex. The nuclear resonance vibrational spectra (NRVS) of 1 and 2 are distinct and provide direct experimental insight into differences in bonding in these complexes. In particular, the symmetric out-of-plane Fe-N-O bending mode is shifted to higher energy by 188 cm-1 in 2 in comparison to 1. Using quantum chemistry centered normal coordinate analysis (QCC-NCA), this is shown to arise from an increase in Fe-NO bond order and a stiffening of the Fe(NO)2 unit upon reduction of 1 to 2. DFT calculations demonstrate that the changes in bonding arise from an iron-centered reduction which leads to a distinct increase in Fe-NO π-back-bonding in {Fe(NO)2}10 DNICs in comparison to the corresponding {Fe(NO)2}9 complexes, in agreement with all experimental findings. Finally, the implications of the electronic structure of DNICs for their reactivity are discussed, especially with respect to N-N bond formation in NO reductases.

UR - https://www.scopus.com/pages/publications/84973345894

UR - https://www.scopus.com/pages/publications/84973345894#tab=citedBy

U2 - 10.1021/acs.inorgchem.6b00510

DO - 10.1021/acs.inorgchem.6b00510

M3 - Article

AN - SCOPUS:84973345894

SN - 0020-1669

VL - 55

SP - 5485

EP - 5501

JO - Inorganic chemistry

JF - Inorganic chemistry

IS - 11

ER -

Unusual Synthetic Pathway for an {Fe(NO)₂}⁹ Dinitrosyl Iron Complex (DNIC) and Insight into DNIC Electronic Structure via Nuclear Resonance Vibrational Spectroscopy

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