Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond
Abstract
Axial Cu–S(Met) bonds in electron transfer (ET) active sites are generally found to lower their reduction potentials. An axial S(Met) bond is also present in cytochrome c (cyt c) and is generally thought to increase the reduction potential. The highly covalent nature of the porphyrin environment in heme proteins precludes using many spectroscopic approaches to directly study the Fe site to experimentally quantify this bond. Alternatively, L-edge X-ray absorption spectroscopy (XAS) enables one to directly focus on the 3d-orbitals in a highly covalent environment and has previously been successfully applied to porphyrin model complexes. However, this technique cannot be extended to metalloproteins in solution. Here, we use metal K-edge XAS to obtain L-edge like data through 1s2p resonance inelastic X-ray scattering (RIXS). It has been applied here to a bis-imidazole porphyrin model complex and cyt c. The RIXS data on the model complex are directly correlated to L-edge XAS data to develop the complementary nature of these two spectroscopic methods. Comparison between the bis-imidazole model complex and cyt c in ferrous and ferric oxidation states show quantitative differences that reflect differences in axial ligand covalency. The data reveal an increased covalency for the S(Met) relative to N(His) axial ligand andmore »
- Authors:
-
- Department of Chemistry, Stanford University, Stanford, California 94305, United States, Linac Coherent Light Source, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, California 94025, United States
- Department of Chemistry, Stanford University, Stanford, California 94305, United States
- Department of Chemistry, Stanford University, Stanford, California 94305, United States, Department of Chemistry — Ångström, Uppsala University, SE-751 20 Uppsala, Sweden
- Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, California 94025, United States
- Linac Coherent Light Source, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, California 94025, United States
- Advanced Photon Source, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, Illinois 60439, United States
- Department of Chemistry, Stanford University, Stanford, California 94305, United States, Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, California 94025, United States
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1179605
- Alternate Identifier(s):
- OSTI ID: 1241044
- Grant/Contract Number:
- AC02-76SF00515; AC02-06CH11357
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- Journal of the American Chemical Society
- Additional Journal Information:
- Journal Name: Journal of the American Chemical Society Journal Volume: 136 Journal Issue: 52; Journal ID: ISSN 0002-7863
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY
Citation Formats
Kroll, Thomas, Hadt, Ryan G., Wilson, Samuel A., Lundberg, Marcus, Yan, James J., Weng, Tsu-Chien, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Casa, Diego, Upton, Mary H., Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond. United States: N. p., 2014.
Web. doi:10.1021/ja5100367.
Kroll, Thomas, Hadt, Ryan G., Wilson, Samuel A., Lundberg, Marcus, Yan, James J., Weng, Tsu-Chien, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Casa, Diego, Upton, Mary H., Hedman, Britt, Hodgson, Keith O., & Solomon, Edward I. Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond. United States. https://doi.org/10.1021/ja5100367
Kroll, Thomas, Hadt, Ryan G., Wilson, Samuel A., Lundberg, Marcus, Yan, James J., Weng, Tsu-Chien, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Casa, Diego, Upton, Mary H., Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. 2014.
"Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond". United States. https://doi.org/10.1021/ja5100367.
@article{osti_1179605,
title = {Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c : Nature and Role of the Axial Methionine–Fe Bond},
author = {Kroll, Thomas and Hadt, Ryan G. and Wilson, Samuel A. and Lundberg, Marcus and Yan, James J. and Weng, Tsu-Chien and Sokaras, Dimosthenis and Alonso-Mori, Roberto and Casa, Diego and Upton, Mary H. and Hedman, Britt and Hodgson, Keith O. and Solomon, Edward I.},
abstractNote = {Axial Cu–S(Met) bonds in electron transfer (ET) active sites are generally found to lower their reduction potentials. An axial S(Met) bond is also present in cytochrome c (cyt c) and is generally thought to increase the reduction potential. The highly covalent nature of the porphyrin environment in heme proteins precludes using many spectroscopic approaches to directly study the Fe site to experimentally quantify this bond. Alternatively, L-edge X-ray absorption spectroscopy (XAS) enables one to directly focus on the 3d-orbitals in a highly covalent environment and has previously been successfully applied to porphyrin model complexes. However, this technique cannot be extended to metalloproteins in solution. Here, we use metal K-edge XAS to obtain L-edge like data through 1s2p resonance inelastic X-ray scattering (RIXS). It has been applied here to a bis-imidazole porphyrin model complex and cyt c. The RIXS data on the model complex are directly correlated to L-edge XAS data to develop the complementary nature of these two spectroscopic methods. Comparison between the bis-imidazole model complex and cyt c in ferrous and ferric oxidation states show quantitative differences that reflect differences in axial ligand covalency. The data reveal an increased covalency for the S(Met) relative to N(His) axial ligand and a higher degree of covalency for the ferric states relative to the ferrous states. These results are reproduced by DFT calculations, which are used to evaluate the thermodynamics of the Fe–S(Met) bond and its dependence on redox state. Furthermore, these results provide insight into a number of previous chemical and physical results on cyt c.},
doi = {10.1021/ja5100367},
url = {https://www.osti.gov/biblio/1179605},
journal = {Journal of the American Chemical Society},
issn = {0002-7863},
number = 52,
volume = 136,
place = {United States},
year = {Thu Dec 18 00:00:00 EST 2014},
month = {Thu Dec 18 00:00:00 EST 2014}
}
Web of Science
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