Experimental electronic structures of the FeIV=O bond in S=1 heme vs. nonheme sites: Effect of the porphyrin ligand

Braun, Augustin; Gee, Leland B.; Waters, Max D. J.; Jose, Anex; Baker, Michael L.; Mara, Michael W.; Babicz, Jr., Jeffrey T.; Ehudin, Melanie A.; Quist, David A.; Zhou, Ang; Kroll, Thomas; Titus, Charles J.; Lee, Sang-Jun; Nordlund, Dennis; Sokaras, Dimosthenis; Yoda, Yoshitaka; Kobayashi, Yasuhiro; Tamasaku, Kenji; Hedman, Britt; Hodgson, Keith O.; Karlin, Kenneth D.; Que. Jr., Lawrence; Solomon, Edward I.

doi:10.1073/pnas.2420205122

Title: Experimental electronic structures of the Fe^IV=O bond in S=1 heme vs. nonheme sites: Effect of the porphyrin ligand

Journal Article · Fri Feb 21 00:00:00 UTC 2025 · Proceedings of the National Academy of Sciences

DOI: https://doi.org/10.1073/pnas.2420205122 · OSTI ID:2587857

^[1]; Gee, Leland B. ^[1];

^[2];

^[3]; Mara, Michael W. ^[4];

^[2]; Ehudin, Melanie A. ^[5];

^[5]; Zhou, Ang ^[6]; Kroll, Thomas ^[7];

^[7];

^[7]; Nordlund, Dennis ^[7];

^[7]; Yoda, Yoshitaka ^[8];

^[9]; Tamasaku, Kenji ^[10]; Hedman, Britt ^[7];

^[7] more »

Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Stanford Univ., CA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); Univ. of Manchester (United Kingdom); Harwell Science and Innovation Campus, Didcot (United Kingdom). Diamond Light Source, Ltd.
Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); Argonne National Laboratory (ANL), Argonne, IL (United States)
Johns Hopkins Univ., Baltimore, MD (United States)
Univ. of Minnesota, Minneapolis, MN (United States)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); Stanford Univ., CA (United States)
Japan Synchrotron Radiation Research Institute, Sayo, Hyogo (Japan)
Kyoto Univ. (Japan)
RIKEN SPring-8 Center, Sayo (Japan)

High-valent Fe^IV=O species are common intermediates in biological and artificial catalysts. Heme and nonheme S=1 Fe^IV=O sites have been synthesized and studied for decades but little quantitative experimental comparison of their electronic structures has been available, due to the lack of direct methods focused on the iron. This study allows a rigorous determination of the electronic structure of a nonheme Fe^IV=O center and its comparison to an Fe^IV=O heme site using 1s2p resonant inelastic X-ray scattering (RIXS) and Fe L-edge X-ray absorption spectroscopy (XAS). Further, variable temperature magnetic circular dichroism (VT-MCD) of the ligand field transitions, combined with nuclear resonance vibrational spectroscopy of the two S=1 Fe^IV=O systems show that the equatorial ligand field decreases from a nonheme to a heme Fe^IV=O site. Alternatively, RIXS and Fe L-edge XAS combined with MCD show that the Fe dπ orbitals are unperturbed in the Fe^IV=O heme relative to the nonheme site because the strong axial Fe-O bond uncouples the Fe dπ orbitals from the porphyrin π-system. As a consequence, the thermodynamics and kinetics of the H-atom abstraction reactions are actually very similar for heme compound II and nonheme Fe^IV=O active sites.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2587857

Journal Information:: Proceedings of the National Academy of Sciences, Journal Name: Proceedings of the National Academy of Sciences Journal Issue: 8 Vol. 122; ISSN 1091-6490; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

Enhanced Reactivities of Iron(IV)‐Oxo Porphyrin Species in Oxidation Reactions Promoted by Intramolecular Hydrogen‐Bonding Gong, Zhe; Wang, Liwei; Xu, Yiran Advanced Science, Vol. 11, Issue 19 https://doi.org/10.1002/advs.202310333	journal	March 2024
Comparison of FeIV?O Heme and Non-heme Species: Electronic Structures, Bonding, and Reactivities Decker, Andrea; Solomon, Edward I. Angewandte Chemie International Edition, Vol. 44, Issue 15 https://doi.org/10.1002/anie.200462182	journal	April 2005
A Combined NRVS and DFT Study of Fe ^IV O Model Complexes: A Diagnostic Method for the Elucidation of Non-Heme Iron Enzyme Intermediates Bell, Caleb B.; Wong, Shaun D.; Xiao, Yuming Angewandte Chemie International Edition, Vol. 47, Issue 47 https://doi.org/10.1002/anie.200803740	journal	November 2008
A Synthetic High-Spin Oxoiron(IV) Complex: Generation, Spectroscopic Characterization, and Reactivity England, Jason; Martinho, Marlène; Farquhar, Erik R. Angewandte Chemie International Edition, Vol. 48, Issue 20 https://doi.org/10.1002/anie.200900863	journal	May 2009
Nuclear Resonance Vibrational Spectroscopy on the FeIVO S=2 Non-Heme Site in TMG3tren: Experimentally Calibrated Insights into Reactivity Wong, Shaun D.; Bell, Caleb B.; Liu, Lei V. Angewandte Chemie International Edition, Vol. 50, Issue 14 https://doi.org/10.1002/anie.201007692	journal	March 2011
Driving Force for Oxygen-Atom Transfer by Heme-Thiolate Enzymes Wang, Xiaoshi; Peter, Sebastian; Ullrich, René Angewandte Chemie International Edition, Vol. 52, Issue 35 https://doi.org/10.1002/anie.201302137	journal	July 2013
The ORCA program system: The ORCA program system Neese, Frank Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 2, Issue 1 https://doi.org/10.1002/wcms.81	journal	June 2011
Cytochromes P450 and metabolism of xenobiotics Anzenbacher, P.; Anzenbacherová, E. Cellular and Molecular Life Sciences, Vol. 58, Issue 5 https://doi.org/10.1007/PL00000897	journal	May 2001
Horseradish peroxidase compound I: evidence for spin coupling between the heme iron and a ‘free’ radical Schulz, C. E.; Devaney, P. W.; Winkler, H. FEBS Letters, Vol. 103, Issue 1 https://doi.org/10.1016/0014-5793(79)81259-4	journal	July 1979
Resonance Raman spectroscopic characterizations of horseradish peroxidase. Observations of the FeIV = O stretching vibration of Compound II Terner, James; Sitter, Andrew J.; Reczek, Catherine M. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 828, Issue 1 https://doi.org/10.1016/0167-4838(85)90011-1	journal	March 1985
Electronic structure and reactivity of high-valent oxo iron porphyrins Fujii, Hiroshi Coordination Chemistry Reviews, Vol. 226, Issue 1-2 https://doi.org/10.1016/S0010-8545(01)00441-6	journal	March 2002
Prediction and interpretation of the 57Fe isomer shift in Mössbauer spectra by density functional theory Neese, Frank Inorganica Chimica Acta, Vol. 337 https://doi.org/10.1016/S0020-1693(02)01031-9	journal	September 2002
Multiplet effects in X-ray spectroscopy Groot, Frank de Coordination Chemistry Reviews, Vol. 249, Issue 1-2 https://doi.org/10.1016/j.ccr.2004.03.018	journal	January 2005
Oxidative dealkylation DNA repair mediated by the mononuclear non-heme iron AlkB proteins Mishina, Yukiko; He, Chuan Journal of Inorganic Biochemistry, Vol. 100, Issue 4 https://doi.org/10.1016/j.jinorgbio.2005.12.018	journal	April 2006
Resonance Raman spectroscopy of oxoiron(IV) porphyrin π-cation radical and oxoiron(IV) hemes in peroxidase intermediates Terner, James; Palaniappan, Vaithianathan; Gold, Avram Journal of Inorganic Biochemistry, Vol. 100, Issue 4 https://doi.org/10.1016/j.jinorgbio.2006.01.008	journal	April 2006
High-valent iron in chemical and biological oxidations Groves, John T. Journal of Inorganic Biochemistry, Vol. 100, Issue 4 https://doi.org/10.1016/j.jinorgbio.2006.01.012	journal	April 2006
Synthetic Mononuclear Nonheme Iron–Oxygen Intermediates Nam, Wonwoo Accounts of Chemical Research, Vol. 48, Issue 8 https://doi.org/10.1021/acs.accounts.5b00218	journal	July 2015
Toward the Synthesis of More Reactive S = 2 Non-Heme Oxoiron(IV) Complexes Puri, Mayank; Que, Lawrence Accounts of Chemical Research, Vol. 48, Issue 8 https://doi.org/10.1021/acs.accounts.5b00244	journal	July 2015
Mechanisms of O₂ Activation by Mononuclear Non-Heme Iron Enzymes Solomon, Edward I.; DeWeese, Dory E.; Babicz, Jeffrey T. Biochemistry, Vol. 60, Issue 46 https://doi.org/10.1021/acs.biochem.1c00370	journal	July 2021
Discussing the Terms Biomimetic and Bioinspired within Bioinorganic Chemistry Engbers, Silène; van Langevelde, Phebe H.; Hetterscheid, Dennis G. H. Inorganic Chemistry, Vol. 63, Issue 43 https://doi.org/10.1021/acs.inorgchem.4c01070	journal	September 2024
Heme and Nonheme High-Valent Iron and Manganese Oxo Cores in Biological and Abiological Oxidation Reactions Guo, Mian; Corona, Teresa; Ray, Kallol ACS Central Science, Vol. 5, Issue 1 https://doi.org/10.1021/acscentsci.8b00698	journal	December 2018
Moessbauer and electron paramagnetic resonance studies of horseradish peroxidase and its catalytic intermediates Schulz, C. E.; Rutter, R.; Sage, J. T. Biochemistry, Vol. 23, Issue 20 https://doi.org/10.1021/bi00315a033	journal	September 1984
Time-resolved and static resonance Raman spectroscopy of horseradish peroxidase intermediates Oertling, W. Anthony; Babcock, Gerald T. Biochemistry, Vol. 27, Issue 9 https://doi.org/10.1021/bi00409a032	journal	May 1988
The First Direct Characterization of a High-Valent Iron Intermediate in the Reaction of an α-Ketoglutarate-Dependent Dioxygenase: A High-Spin Fe(IV) Complex in Taurine/α-Ketoglutarate Dioxygenase (TauD) from Escherichia coli ^† Price, John C.; Barr, Eric W.; Tirupati, Bhramara Biochemistry, Vol. 42, Issue 24 https://doi.org/10.1021/bi030011f	journal	June 2003
Heme Enzyme Structure and Function Poulos, Thomas L. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr400415k	journal	January 2014
MCD C -Term Signs, Saturation Behavior, and Determination of Band Polarizations in Randomly Oriented Systems with Spin S ≥ ¹ / ₂ . Applications to S = ¹ / ₂ and S = ⁵ / ₂ Neese, Frank; Solomon, Edward I. Inorganic Chemistry, Vol. 38, Issue 8 https://doi.org/10.1021/ic981264d	journal	April 1999
Electronic structure of plastocyanin: excited state spectral features Gewirth, Andrew A.; Solomon, Edward I. Journal of the American Chemical Society, Vol. 110, Issue 12 https://doi.org/10.1021/ja00220a015	journal	June 1988
Structural characterization of horseradish peroxidase using EXAFS spectroscopy. Evidence for Fe = O ligation in compounds I and II Penner-Hahn, James E.; Smith Eble, Kim.; McMurry, Thomas J. Journal of the American Chemical Society, Vol. 108, Issue 24 https://doi.org/10.1021/ja00284a054	journal	November 1986
Oxygenation patterns for iron(II) porphyrins. Peroxo and ferryl (FeIVO) intermediates detected by proton nuclear magnetic resonance spectroscopy during the oxygenation of (tetramesitylporphyrin)iron(II) Balch, Alan L.; Chan, Yee Wai; Cheng, Ru Jen Journal of the American Chemical Society, Vol. 106, Issue 25 https://doi.org/10.1021/ja00337a022	journal	December 1984
High-valent iron-porphyrin complexes related to peroxidase and cytochrome P-450 Groves, John T.; Haushalter, Robert C.; Nakamura, Mikio Journal of the American Chemical Society, Vol. 103, Issue 10 https://doi.org/10.1021/ja00400a075	journal	May 1981
Formation of porphyrin ferryl (FeO2+) complexes through the addition of nitrogen bases to peroxo-bridged iron(III) porphyrins Chin, Der-Hang; Balch, Alan L.; La Mar, Gerd N. Journal of the American Chemical Society, Vol. 102, Issue 4 https://doi.org/10.1021/ja00524a051	journal	February 1980
L-edge X-ray Absorption Spectroscopy of Non-Heme Iron Sites: Experimental Determination of Differential Orbital Covalency Wasinger, Erik C.; de Groot, Frank M. F.; Hedman, Britt Journal of the American Chemical Society, Vol. 125, Issue 42 https://doi.org/10.1021/ja034634s	journal	October 2003
Nonheme Fe ^IV O Complexes That Can Oxidize the C−H Bonds of Cyclohexane at Room Temperature Kaizer, József; Klinker, Eric J.; Oh, Na Young Journal of the American Chemical Society, Vol. 126, Issue 2 https://doi.org/10.1021/ja037288n	journal	January 2004
Direct Detection of Oxygen Intermediates in the Non-Heme Fe Enzyme Taurine/α-Ketoglutarate Dioxygenase Proshlyakov, Denis A.; Henshaw, Timothy F.; Monterosso, Greta R. Journal of the American Chemical Society, Vol. 126, Issue 4 https://doi.org/10.1021/ja039113j	journal	February 2004
EXAFS Spectroscopic Evidence for an Fe═O Unit in the Fe(IV) Intermediate Observed during Oxygen Activation by Taurine:α-Ketoglutarate Dioxygenase Riggs-Gelasco, Pamela J.; Price, John C.; Guyer, Robert B. Journal of the American Chemical Society, Vol. 126, Issue 26 https://doi.org/10.1021/ja048255q	journal	June 2004
Fe L-Edge X-ray Absorption Spectroscopy of Low-Spin Heme Relative to Non-heme Fe Complexes: Delocalization of Fe d-Electrons into the Porphyrin Ligand Hocking, Rosalie K.; Wasinger, Erik C.; Yan, Yi-Long Journal of the American Chemical Society, Vol. 129, Issue 1 https://doi.org/10.1021/ja065627h	journal	January 2007
Spectroscopic and Quantum Chemical Studies on Low-Spin Fe ^IV O Complexes: Fe−O Bonding and Its Contributions to Reactivity Decker, Andrea; Rohde, Jan-Uwe; Klinker, Eric J. Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja074900s	journal	December 2007
Formation, Structure, and EPR Detection of a High Spin Fe ^IV —Oxo Species Derived from Either an Fe ^III —Oxo or Fe ^III —OH Complex Lacy, David C.; Gupta, Rupal; Stone, Kari L. Journal of the American Chemical Society, Vol. 132, Issue 35 https://doi.org/10.1021/ja1047818	journal	September 2010
Modeling TauD- J : A High-Spin Nonheme Oxoiron(IV) Complex with High Reactivity toward C–H Bonds Biswas, Achintesh N.; Puri, Mayank; Meier, Katlyn K. Journal of the American Chemical Society, Vol. 137, Issue 7 https://doi.org/10.1021/ja511757j	journal	February 2015
The Molecular Mechanism of the Catalase Reaction Alfonso-Prieto, Mercedes; Biarnés, Xevi; Vidossich, Pietro Journal of the American Chemical Society, Vol. 131, Issue 33 https://doi.org/10.1021/ja9018572	journal	August 2009
S K-edge XAS and DFT Calculations on Cytochrome P450: Covalent and Ionic Contributions to the Cysteine-Fe Bond and Their Contribution to Reactivity Dey, Abhishek; Jiang, Yonging; Ortiz de Montellano, Paul Journal of the American Chemical Society, Vol. 131, Issue 22 https://doi.org/10.1021/ja901868q	journal	June 2009
A Multiplet Analysis of Fe K-Edge 1s → 3d Pre-Edge Features of Iron Complexes Westre, Tami E.; Kennepohl, Pierre; DeWitt, Jane G. Journal of the American Chemical Society, Vol. 119, Issue 27 https://doi.org/10.1021/ja964352a	journal	July 1997
Nuclear Resonance Vibrational Spectroscopic Definition of the Facial Triad Fe ^IV ═O Intermediate in Taurine Dioxygenase: Evaluation of Structural Contributions to Hydrogen Atom Abstraction Srnec, Martin; Iyer, Shyam R.; Dassama, Laura M. K. Journal of the American Chemical Society, Vol. 142, Issue 44 https://doi.org/10.1021/jacs.0c08903	journal	October 2020
Modeling Non-Heme Iron Halogenases: High-Spin Oxoiron(IV)–Halide Complexes That Halogenate C–H Bonds Puri, Mayank; Biswas, Achintesh N.; Fan, Ruixi Journal of the American Chemical Society, Vol. 138, Issue 8 https://doi.org/10.1021/jacs.5b11511	journal	February 2016
Activation of Dioxygen by Iron and Manganese Complexes: A Heme and Nonheme Perspective Sahu, Sumit; Goldberg, David P. Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b05251	journal	August 2016
Tuning the Geometric and Electronic Structure of Synthetic High-Valent Heme Iron(IV)-Oxo Models in the Presence of a Lewis Acid and Various Axial Ligands Ehudin, Melanie A.; Gee, Leland B.; Sabuncu, Sinan Journal of the American Chemical Society, Vol. 141, Issue 14 https://doi.org/10.1021/jacs.9b00795	journal	March 2019
Enhanced Rates of C–H Bond Cleavage by a Hydrogen-Bonded Synthetic Heme High-Valent Iron(IV) Oxo Complex Ehudin, Melanie A.; Quist, David A.; Karlin, Kenneth D. Journal of the American Chemical Society, Vol. 141, Issue 32 https://doi.org/10.1021/jacs.9b01253	journal	July 2019
Prediction of Iron K-Edge Absorption Spectra Using Time-Dependent Density Functional Theory ^† DeBeer George, Serena; Petrenko, Taras; Neese, Frank The Journal of Physical Chemistry A, Vol. 112, Issue 50 https://doi.org/10.1021/jp803174m	journal	December 2008
Elucidation of the Fe(iv)=O intermediate in the catalytic cycle of the halogenase SyrB2 Wong, Shaun D.; Srnec, Martin; Matthews, Megan L. Nature, Vol. 499, Issue 7458 https://doi.org/10.1038/nature12304	journal	July 2013
The biology and chemistry of high-valent iron–oxo and iron–nitrido complexes Hohenberger, Johannes; Ray, Kallol; Meyer, Karsten Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1718	journal	January 2012
Prediction of high-valent iron K-edge absorption spectra by time-dependent Density Functional Theory Chandrasekaran, P.; Stieber, S. Chantal E.; Collins, Terrence J. Dalton Transactions, Vol. 40, Issue 42 https://doi.org/10.1039/c1dt11331c	journal	January 2011
The biosynthesis of penicillins and cephalosporins Baldwin, J. E.; Abraham, Edward Natural Product Reports, Vol. 5, Issue 2 https://doi.org/10.1039/np9880500129	journal	January 1988
Multiplet calculations of L _2,3 x-ray absorption near-edge structures for 3d transition-metal compounds Ikeno, Hidekazu; de Groot, Frank M. F.; Stavitski, Eli Journal of Physics: Condensed Matter, Vol. 21, Issue 10 https://doi.org/10.1088/0953-8984/21/10/104208	journal	February 2009
Cytochrome P450 Compound I: Capture, Characterization, and C-H Bond Activation Kinetics Rittle, J.; Green, M. T. Science, Vol. 330, Issue 6006 https://doi.org/10.1126/science.1193478	journal	November 2010
Iron(IV)hydroxide pKa and the Role of Thiolate Ligation in C-H Bond Activation by Cytochrome P450 Yosca, T. H.; Rittle, J.; Krest, C. M. Science, Vol. 342, Issue 6160 https://doi.org/10.1126/science.1244373	journal	November 2013
The Theory of Atomic Structure and Spectra Cowan, Robert D. Los Alamos Series in Basic and Applied Sciences, Vol. 3 https://doi.org/10.1525/9780520906150	book	December 1981

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Title: Experimental electronic structures of the Fe^IV=O bond in S=1 heme vs. nonheme sites: Effect of the porphyrin ligand