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Title: Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy

Abstract

The size and complexity of Mo-dependent nitrogenase, a multicomponent enzyme capable of reducing dinitrogen to ammonia, have made a detailed understanding of the FeMo cofactor (FeMoco) active site electronic structure an ongoing challenge. Selective substitution of sulfur by selenium in FeMoco affords a unique probe wherein local Fe-Se interactions can be directly interrogated via high-energy resolution fluorescence detected X-ray absorption spectroscopic (HERFD XAS) and extended X-ray absorption fine structure (EXAFS) studies. These studies reveal a significant asymmetry in the electronic distribution of the FeMoco, suggesting a more localized electronic structure picture than is typically assumed for iron-sulfur clusters. Supported by experimental small molecule model data in combination with time dependent density functional theory (TDDFT) calculations, the HERFD XAS data is consistent with an assignment of Fe2/Fe6 as an antiferromagnetically coupled diferric pair. HERFD XAS and EXAFS have also been applied to Se-substituted CO-inhibited MoFe protein, demonstrating the ability of these methods to reveal electronic and structural changes that occur upon substrate binding. These results emphasize the utility of Se HERFD XAS and EXAFS for selectively probing the local electronic and geometric structure of FeMoco.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [4]; ORCiD logo [3]; ORCiD logo [5]; ORCiD logo [1]
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  1. Max Planck Institute for Chemical Energy Conversion, Stiftstr. 34-36, D-45470 Mülheim an der Ruhr, Germany
  2. Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California 91125, United States
  3. PULSE Institute, SLAC National Accelerator Laboratory, Menlo Park, California 94025, United States
  4. Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, California 94025, United States
  5. Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California 91125, United States, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California 91125, United States
Publication Date:
Research Org.:
Max Planck Institute for Chemical Energy Conversion, Mülheim (Germany)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1557383
Alternate Identifier(s):
OSTI ID: 1559864
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Published Article
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Name: Journal of the American Chemical Society Journal Volume: 141 Journal Issue: 34; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Henthorn, Justin T., Arias, Renee J., Koroidov, Sergey, Kroll, Thomas, Sokaras, Dimosthenis, Bergmann, Uwe, Rees, Douglas C., and DeBeer, Serena. Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy. United States: N. p., 2019. Web. doi:10.1021/jacs.9b06988.
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Henthorn, Justin T., Arias, Renee J., Koroidov, Sergey, Kroll, Thomas, Sokaras, Dimosthenis, Bergmann, Uwe, Rees, Douglas C., & DeBeer, Serena. Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy. United States. https://doi.org/10.1021/jacs.9b06988
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Henthorn, Justin T., Arias, Renee J., Koroidov, Sergey, Kroll, Thomas, Sokaras, Dimosthenis, Bergmann, Uwe, Rees, Douglas C., and DeBeer, Serena. Mon . "Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy". United States. https://doi.org/10.1021/jacs.9b06988.
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@article{osti_1557383,
title = {Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy},
author = {Henthorn, Justin T. and Arias, Renee J. and Koroidov, Sergey and Kroll, Thomas and Sokaras, Dimosthenis and Bergmann, Uwe and Rees, Douglas C. and DeBeer, Serena},
abstractNote = {The size and complexity of Mo-dependent nitrogenase, a multicomponent enzyme capable of reducing dinitrogen to ammonia, have made a detailed understanding of the FeMo cofactor (FeMoco) active site electronic structure an ongoing challenge. Selective substitution of sulfur by selenium in FeMoco affords a unique probe wherein local Fe-Se interactions can be directly interrogated via high-energy resolution fluorescence detected X-ray absorption spectroscopic (HERFD XAS) and extended X-ray absorption fine structure (EXAFS) studies. These studies reveal a significant asymmetry in the electronic distribution of the FeMoco, suggesting a more localized electronic structure picture than is typically assumed for iron-sulfur clusters. Supported by experimental small molecule model data in combination with time dependent density functional theory (TDDFT) calculations, the HERFD XAS data is consistent with an assignment of Fe2/Fe6 as an antiferromagnetically coupled diferric pair. HERFD XAS and EXAFS have also been applied to Se-substituted CO-inhibited MoFe protein, demonstrating the ability of these methods to reveal electronic and structural changes that occur upon substrate binding. These results emphasize the utility of Se HERFD XAS and EXAFS for selectively probing the local electronic and geometric structure of FeMoco.},
doi = {10.1021/jacs.9b06988},
journal = {Journal of the American Chemical Society},
number = 34,
volume = 141,
place = {United States},
year = {2019},
month = {7}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/jacs.9b06988
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Citation Metrics:
Cited by: 9 works
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Figures / Tables:

Figure 1 Figure 1: Summary of Se incorporation and migration reactions in FeMoco from A. vinelandii (PDB-IDs 3U7Q, 5BVG, 5BVH). Nitrogen atoms are shown in blue, oxygen atoms in red, and carbon atoms in gray.
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Works referencing / citing this record:

N 2 O Reductase Activity of a [Cu 4 S] Cluster in the 4Cu I Redox State Modulated by Hydrogen Bond Donors and Proton Relays in the Secondary Coordination Sphere
journal, November 2019

  • Hsu, Chia-Wei; Rathnayaka, Suresh C.; Islam, Shahidul M.
  • Angewandte Chemie International Edition, Vol. 59, Issue 2
  • DOI: 10.1002/anie.201906327

N 2 O Reductase Activity of a [Cu 4 S] Cluster in the 4Cu I Redox State Modulated by Hydrogen Bond Donors and Proton Relays in the Secondary Coordination Sphere
journal, November 2019

  • Hsu, Chia-Wei; Rathnayaka, Suresh C.; Islam, Shahidul M.
  • Angewandte Chemie International Edition, Vol. 59, Issue 2
  • DOI: 10.1002/anie.201906327

N 2 O Reductase Activity of a [Cu 4 S] Cluster in the 4Cu I Redox State Modulated by Hydrogen Bond Donors and Proton Relays in the Secondary Coordination Sphere
journal, November 2019

  • Hsu, Chia‐Wei; Rathnayaka, Suresh C.; Islam, Shahidul M.
  • Angewandte Chemie, Vol. 132, Issue 2
  • DOI: 10.1002/ange.201906327

Theory of chemical bonds in metalloenzymes XXIV electronic and spin structures of FeMoco and Fe-S clusters by classical and quantum computing
journal, May 2020

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    Table 1 (p. 4)table
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    Figure 10 (p. 9)figure
    Table 5 (p. 9)table
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