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Resonant inelastic X-ray scattering on ferrous and ferric bis-imidazole porphyrin and cytochrome c: nature and role of the axial methionine-Fe bond

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. (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. Journal of the American Chemical Society, 136 (52). pp. 18087-18099. ISSN 0002-7863. PMCID PMC4291809. doi:10.1021/ja5100367.

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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. These results provide insight into a number of previous chemical and physical results on cyt c.

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URLURL TypeDescription CentralArticle Information
Hadt, Ryan G.0000-0001-6026-1358
Solomon, Edward I.0000-0003-0291-3199
Additional Information:© 2014 American Chemical Society. ACS AuthorChoice - This is an open access article published under an ACS AuthorChoice License, which permits copying and redistribution of the article or any adaptations for non-commercial purposes. Received: October 7, 2014. Published: December 4, 2014. T.K. acknowledges financial support by the German Research Foundation (DFG) grant KR3611/2-1. R.G.H. acknowledges a Gerhard Casper Stanford Graduate Fellowship and the Achievement Rewards for College Scientists Foundation (ARCS). M.L. acknowledges the Marcus and Amalia Wallenberg foundation and the Swedish Research Council. This research was supported by the National Institute of General Medical Sciences of the National Institutes of Health under award number R01GM040392 (E.I.S.), NSF grant CHE-1360046 (E.I.S.) and P41GM103393 (K.O.H). Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). Parts of this work was performed at the Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory, which is supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. We acknowledge Ryan Wilson for the kind provision of computer power, and Matthew Kieber-Emmons for help in the purification and preparation of cyt c samples. The authors declare no competing financial interest.
Funding AgencyGrant Number
Deutsche Forschungsgemeinschaft (DFG)KR3611/2-1
Stanford UniversityUNSPECIFIED
Marcus and Amalia Wallenberg FoundationUNSPECIFIED
Swedish Research CouncilUNSPECIFIED
Department of Energy (DOE)DE-AC02-76SF00515
Department of Energy (DOE)DE-AC02-06CH11357
Issue or Number:52
PubMed Central ID:PMC4291809
Record Number:CaltechAUTHORS:20180612-110306586
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Official Citation:Resonant Inelastic X-ray Scattering on Ferrous and Ferric Bis-imidazole Porphyrin and Cytochrome c: Nature and Role of the Axial Methionine–Fe Bond. Thomas Kroll, Ryan G. Hadt, Samuel A. Wilson, Marcus Lundberg, James J. Yan, Tsu-Chien Weng, Dimosthenis Sokaras, Roberto Alonso-Mori, Diego Casa, Mary H. Upton, Britt Hedman, Keith O. Hodgson, and Edward I. Solomon. Journal of the American Chemical Society 2014 136 (52), 18087-18099. DOI: 10.1021/ja5100367
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:87002
Deposited By: George Porter
Deposited On:12 Jun 2018 18:16
Last Modified:15 Nov 2021 20:44

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