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

doi:10.1021/jacs.9b06988

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:

^[1];

^[2]; Koroidov, Sergey ^[3]; Kroll, Thomas ^[4]; Sokaras, Dimosthenis ^[4];

^[3];

^[5];

^[1]

Max Planck Institute for Chemical Energy Conversion, Stiftstr. 34-36, D-45470 Mülheim an der Ruhr, Germany
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, California 91125, United States
PULSE Institute, SLAC National Accelerator Laboratory, Menlo Park, California 94025, United States
Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, California 94025, United States
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:: 2019-07-29

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.  doi: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.  doi: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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DOI: https://doi.org/10.1021/jacs.9b06988

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Theory of chemical bonds in metalloenzymes XXIV electronic and spin structures of FeMoco and Fe-S clusters by classical and quantum computing
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Title: Localized Electronic Structure of Nitrogenase FeMoco Revealed by Selenium K-Edge High Resolution X-ray Absorption Spectroscopy

Abstract

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