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Title: What Is the Right Level of Activation of a High-Spin {FeNO}7Complex to Enable Direct N–N Coupling? Mechanistic Insight into Flavodiiron NO Reductases

Abstract

Flavodiiron nitric oxide reductases (FNORs), found in pathogenic bacteria, are capable of reducing nitric oxide (NO) to nitrous oxide (N2O) to detoxify NO released by the human immune system. Previously, we reported the first FNOR model system that mediates direct NO reduction (Dong, H. T.; et al. J. Am. Chem. Soc. 2018, 140, 13429-13440), but no intermediate of the reaction could be characterized. Here, we present a new set of model complexes that, depending on the ligand substitution, can either mediate direct NO reduction or stabilize a highly activated high-spin (hs) {FeNO}7 complex, the first intermediate of the reaction. The precursors, [{FeII(MPA-(RPhO)2)}2] (1, R = H and 2, R = tBu, Me), were prepared first and fully characterized. Complex 1 (without steric protection) directly reduces NO to N2O almost quantitatively, which constitutes only the second example of this reaction in model systems. Contrarily, the reaction of sterically protected 2 with NO forms the stable mononitrosyl complex 3, which shows one of the lowest N-O stretching frequencies (1689 cm-1) observed so far for a mononuclear hs-{FeNO}7 complex. Here this study confirms that an N-O stretch & LE;1700 cm-1 represents the appropriate level of activation of the FeNO unit to enable directmore » NO reduction. The higher activation level of these hs-{FeNO}7 complexes required for NO reduction compared to those formed in FNORs emphasizes the importance of hydrogen bonding residues in the active sites of FNORs to activate the bound NO ligands for direct N-N coupling and N2O formation. The implications of these results for FNORs are further discussed.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [1];  [3]; ORCiD logo [3];  [3]; ORCiD logo [2]; ORCiD logo [1]
  1. University of Michigan, Ann Arbor, MI (United States)
  2. Pennsylvania State University, University Park, PA (United States)
  3. Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); National Institutes of Health (NIH); USDOE Office of Science (SC)
OSTI Identifier:
1970716
Grant/Contract Number:  
AC02-06CH11357; CHE-2002885; R35 GM-127079; CHE-0840456
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 144; Journal Issue: 36; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Dong, Hai T., Camarena, Stephanie, Sil, Debangsu, Lengel, Michael O., Zhao, Jiyong, Hu, Michael Y., Alp, E. Ercan, Krebs, Carsten, and Lehnert, Nicolai. What Is the Right Level of Activation of a High-Spin {FeNO}7Complex to Enable Direct N–N Coupling? Mechanistic Insight into Flavodiiron NO Reductases. United States: N. p., 2022. Web. doi:10.1021/jacs.2c04292.
Dong, Hai T., Camarena, Stephanie, Sil, Debangsu, Lengel, Michael O., Zhao, Jiyong, Hu, Michael Y., Alp, E. Ercan, Krebs, Carsten, & Lehnert, Nicolai. What Is the Right Level of Activation of a High-Spin {FeNO}7Complex to Enable Direct N–N Coupling? Mechanistic Insight into Flavodiiron NO Reductases. United States. https://doi.org/10.1021/jacs.2c04292
Dong, Hai T., Camarena, Stephanie, Sil, Debangsu, Lengel, Michael O., Zhao, Jiyong, Hu, Michael Y., Alp, E. Ercan, Krebs, Carsten, and Lehnert, Nicolai. Tue . "What Is the Right Level of Activation of a High-Spin {FeNO}7Complex to Enable Direct N–N Coupling? Mechanistic Insight into Flavodiiron NO Reductases". United States. https://doi.org/10.1021/jacs.2c04292. https://www.osti.gov/servlets/purl/1970716.
@article{osti_1970716,
title = {What Is the Right Level of Activation of a High-Spin {FeNO}7Complex to Enable Direct N–N Coupling? Mechanistic Insight into Flavodiiron NO Reductases},
author = {Dong, Hai T. and Camarena, Stephanie and Sil, Debangsu and Lengel, Michael O. and Zhao, Jiyong and Hu, Michael Y. and Alp, E. Ercan and Krebs, Carsten and Lehnert, Nicolai},
abstractNote = {Flavodiiron nitric oxide reductases (FNORs), found in pathogenic bacteria, are capable of reducing nitric oxide (NO) to nitrous oxide (N2O) to detoxify NO released by the human immune system. Previously, we reported the first FNOR model system that mediates direct NO reduction (Dong, H. T.; et al. J. Am. Chem. Soc. 2018, 140, 13429-13440), but no intermediate of the reaction could be characterized. Here, we present a new set of model complexes that, depending on the ligand substitution, can either mediate direct NO reduction or stabilize a highly activated high-spin (hs) {FeNO}7 complex, the first intermediate of the reaction. The precursors, [{FeII(MPA-(RPhO)2)}2] (1, R = H and 2, R = tBu, Me), were prepared first and fully characterized. Complex 1 (without steric protection) directly reduces NO to N2O almost quantitatively, which constitutes only the second example of this reaction in model systems. Contrarily, the reaction of sterically protected 2 with NO forms the stable mononitrosyl complex 3, which shows one of the lowest N-O stretching frequencies (1689 cm-1) observed so far for a mononuclear hs-{FeNO}7 complex. Here this study confirms that an N-O stretch & LE;1700 cm-1 represents the appropriate level of activation of the FeNO unit to enable direct NO reduction. The higher activation level of these hs-{FeNO}7 complexes required for NO reduction compared to those formed in FNORs emphasizes the importance of hydrogen bonding residues in the active sites of FNORs to activate the bound NO ligands for direct N-N coupling and N2O formation. The implications of these results for FNORs are further discussed.},
doi = {10.1021/jacs.2c04292},
journal = {Journal of the American Chemical Society},
number = 36,
volume = 144,
place = {United States},
year = {Tue Aug 30 00:00:00 EDT 2022},
month = {Tue Aug 30 00:00:00 EDT 2022}
}

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