skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The Semireduced Mechanism for Nitric Oxide Reduction by Non-Heme Diiron Complexes: Modeling Flavodiiron Nitric Oxide Reductases

Abstract

Flavodiiron nitric oxide reductases (FNORs) are a subclass of Favodiiron proteins (FDPs) capable of preferential binding and subsequent reduction of NO to N2O. FNORs are found in certain pathogenic bacteria, equipping them with resistance to nitrosative stress, generated as a part of the immune defense in humans, and allowing them to proliferate. Here, we report the spectroscopic characterization and detailed reactivity studies of the diiron dinitrosyl model complex [Fe2(BPMP)(OPr)(NO)2](OTf)2 for the FNOR active site that is capable of reducing NO to N2O [Zheng et al., J. Am. Chem. Soc. 2013, 135, 4902-4905]. Using UV-vis spectroscopy, cyclic voltammetry, and spectro-electrochemis- try, we show that one reductive equivalent is in fact sufficient for the quantitative generation of N2O, following a semi-reduced reaction mechanism. This reaction is very efficient and produces N2O with a first-order rate constant k > 102 s-1. Further isotope labeling studies confirm an intramolecular N-N coupling mechanism, consistent with the rapid time scale of the reduction and a very low barrier for N-N bond formation. Accordingly, the reaction proceeds at -80 °C, allowing for the direct observation of the mixed-valent product of the reaction. At higher temperatures, the initial reaction product is unstable and decays, ultimately generating the diferrousmore » complex [Fe2(BPMP)(OPr)2](OTf) and an unidentified ferric product. Finally, these results combined offer deep insight into the mechanism of NO reduction by the relevant model complex [Fe2(BPMP)(OPr)(NO)2]2+ and provide direct evidence that the semireduced mechanism would constitute a highly efficient pathway to accomplish NO reduction to N2O in FNORs and in synthetic catalysts.« less

Authors:
 [1];  [1];  [2];  [2]; ORCiD logo [2];  [1];  [3];  [3];  [3]; ORCiD logo [1]
  1. Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Chemistry
  2. Univ. of Göttingen, Göttingen (Germany). Inst. für Anorganische Chemie
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); USDOE Office of Science (SC)
OSTI Identifier:
1461298
Grant/Contract Number:  
AC02-06CH11357; CHE-0840456
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 140; Journal Issue: 7; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

White, Corey J., Speelman, Amy L., Kupper, Claudia, Demeshko, Serhiy, Meyer, Franc, Shanahan, James P., Alp, E. Ercan, Hu, Michael, Zhao, Jiyong, and Lehnert, Nicolai. The Semireduced Mechanism for Nitric Oxide Reduction by Non-Heme Diiron Complexes: Modeling Flavodiiron Nitric Oxide Reductases. United States: N. p., 2018. Web. doi:10.1021/jacs.7b11464.
White, Corey J., Speelman, Amy L., Kupper, Claudia, Demeshko, Serhiy, Meyer, Franc, Shanahan, James P., Alp, E. Ercan, Hu, Michael, Zhao, Jiyong, & Lehnert, Nicolai. The Semireduced Mechanism for Nitric Oxide Reduction by Non-Heme Diiron Complexes: Modeling Flavodiiron Nitric Oxide Reductases. United States. doi:10.1021/jacs.7b11464.
White, Corey J., Speelman, Amy L., Kupper, Claudia, Demeshko, Serhiy, Meyer, Franc, Shanahan, James P., Alp, E. Ercan, Hu, Michael, Zhao, Jiyong, and Lehnert, Nicolai. Fri . "The Semireduced Mechanism for Nitric Oxide Reduction by Non-Heme Diiron Complexes: Modeling Flavodiiron Nitric Oxide Reductases". United States. doi:10.1021/jacs.7b11464. https://www.osti.gov/servlets/purl/1461298.
@article{osti_1461298,
title = {The Semireduced Mechanism for Nitric Oxide Reduction by Non-Heme Diiron Complexes: Modeling Flavodiiron Nitric Oxide Reductases},
author = {White, Corey J. and Speelman, Amy L. and Kupper, Claudia and Demeshko, Serhiy and Meyer, Franc and Shanahan, James P. and Alp, E. Ercan and Hu, Michael and Zhao, Jiyong and Lehnert, Nicolai},
abstractNote = {Flavodiiron nitric oxide reductases (FNORs) are a subclass of Favodiiron proteins (FDPs) capable of preferential binding and subsequent reduction of NO to N2O. FNORs are found in certain pathogenic bacteria, equipping them with resistance to nitrosative stress, generated as a part of the immune defense in humans, and allowing them to proliferate. Here, we report the spectroscopic characterization and detailed reactivity studies of the diiron dinitrosyl model complex [Fe2(BPMP)(OPr)(NO)2](OTf)2 for the FNOR active site that is capable of reducing NO to N2O [Zheng et al., J. Am. Chem. Soc. 2013, 135, 4902-4905]. Using UV-vis spectroscopy, cyclic voltammetry, and spectro-electrochemis- try, we show that one reductive equivalent is in fact sufficient for the quantitative generation of N2O, following a semi-reduced reaction mechanism. This reaction is very efficient and produces N2O with a first-order rate constant k > 102 s-1. Further isotope labeling studies confirm an intramolecular N-N coupling mechanism, consistent with the rapid time scale of the reduction and a very low barrier for N-N bond formation. Accordingly, the reaction proceeds at -80 °C, allowing for the direct observation of the mixed-valent product of the reaction. At higher temperatures, the initial reaction product is unstable and decays, ultimately generating the diferrous complex [Fe2(BPMP)(OPr)2](OTf) and an unidentified ferric product. Finally, these results combined offer deep insight into the mechanism of NO reduction by the relevant model complex [Fe2(BPMP)(OPr)(NO)2]2+ and provide direct evidence that the semireduced mechanism would constitute a highly efficient pathway to accomplish NO reduction to N2O in FNORs and in synthetic catalysts.},
doi = {10.1021/jacs.7b11464},
journal = {Journal of the American Chemical Society},
number = 7,
volume = 140,
place = {United States},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 25 works
Citation information provided by
Web of Science

Save / Share:

Works referencing / citing this record:

Reductive Nitric Oxide Coupling at a Dinickel Core: Isolation of a Key cis -Hyponitrite Intermediate en route to N 2 O Formation
journal, January 2019

  • Ferretti, Eleonora; Dechert, Sebastian; Demeshko, Serhiy
  • Angewandte Chemie International Edition, Vol. 58, Issue 6
  • DOI: 10.1002/anie.201811925

Homochiral iron( ii )-based metal–organic nanotubes: metamagnetism and selective nitric oxide adsorption in a confined channel
journal, January 2019

  • Jia, Jia-Ge; Feng, Jian-Shen; Huang, Xin-Da
  • Chemical Communications, Vol. 55, Issue 19
  • DOI: 10.1039/c9cc00506d

The Fe 2 (NO) 2 Diamond Core: A Unique Structural Motif In Non-Heme Iron-NO Chemistry
journal, October 2019

  • Dong, Hai T.; Speelman, Amy L.; Kozemchak, Claire E.
  • Angewandte Chemie International Edition, Vol. 58, Issue 49
  • DOI: 10.1002/anie.201911968

Reductive Nitric Oxide Coupling at a Dinickel Core: Isolation of a Key cis -Hyponitrite Intermediate en route to N 2 O Formation
journal, January 2019

  • Ferretti, Eleonora; Dechert, Sebastian; Demeshko, Serhiy
  • Angewandte Chemie International Edition, Vol. 58, Issue 6
  • DOI: 10.1002/anie.201811925

The Fe 2 (NO) 2 Diamond Core: A Unique Structural Motif In Non-Heme Iron-NO Chemistry
journal, October 2019

  • Dong, Hai T.; Speelman, Amy L.; Kozemchak, Claire E.
  • Angewandte Chemie International Edition, Vol. 58, Issue 49
  • DOI: 10.1002/anie.201911968

Homochiral iron( ii )-based metal–organic nanotubes: metamagnetism and selective nitric oxide adsorption in a confined channel
journal, January 2019

  • Jia, Jia-Ge; Feng, Jian-Shen; Huang, Xin-Da
  • Chemical Communications, Vol. 55, Issue 19
  • DOI: 10.1039/c9cc00506d

A Nonheme Sulfur-Ligated {FeNO} 6 Complex and Comparison with Redox-Interconvertible {FeNO} 7 and {FeNO} 8 Analogues
journal, September 2018

  • Dey, Aniruddha; Confer, Alex M.; Vilbert, Avery C.
  • Angewandte Chemie, Vol. 130, Issue 41
  • DOI: 10.1002/ange.201806146

Reductive Nitric Oxide Coupling at a Dinickel Core: Isolation of a Key cis ‐Hyponitrite Intermediate en route to N 2 O Formation
journal, January 2019

  • Ferretti, Eleonora; Dechert, Sebastian; Demeshko, Serhiy
  • Angewandte Chemie, Vol. 131, Issue 6
  • DOI: 10.1002/ange.201811925

Origin of Nitric Oxide Reduction Activity in Flavo–Diiron NO Reductase: Key Roles of the Second Coordination Sphere
journal, February 2019


The Fe 2 (NO) 2 Diamond Core: A Unique Structural Motif In Non‐Heme Iron–NO Chemistry
journal, October 2019

  • Dong, Hai T.; Speelman, Amy L.; Kozemchak, Claire E.
  • Angewandte Chemie, Vol. 131, Issue 49
  • DOI: 10.1002/ange.201911968

A Nonheme Sulfur-Ligated {FeNO} 6 Complex and Comparison with Redox-Interconvertible {FeNO} 7 and {FeNO} 8 Analogues
journal, September 2018

  • Dey, Aniruddha; Confer, Alex M.; Vilbert, Avery C.
  • Angewandte Chemie International Edition, Vol. 57, Issue 41
  • DOI: 10.1002/anie.201806146

Nitric oxide reduction forming hyponitrite triggered by metal‐containing complexes
journal, January 2020

  • Wu, Wun‐Yan; Liaw, Wen‐Feng
  • Journal of the Chinese Chemical Society, Vol. 67, Issue 2
  • DOI: 10.1002/jccs.201900473