L-Edge X-ray Absorption Spectroscopic Investigation of {FeNO}6: Delocalization vs Antiferromagnetic Coupling.

NO is a classic non-innocent ligand, and iron nitrosyls can have different electronic structure descriptions depending on their spin state and coordination environment. These highly covalent ligands are found in metalloproteins and are also used as models for Fe-O2 systems. This study utilizes iron L-edge X-ray absorption spectroscopy (XAS), interpreted using a valence bond configuration interaction multiplet model, to directly experimentally probe the electronic structure of the S = 0 {FeNO}6 compound [Fe(PaPy3)NO]2+ (PaPy3 = N,N-bis(2-pyridylmethyl)amine-N-ethyl-2-pyridine-2-carboxamide) and the S = 0 [Fe(PaPy3)CO]+ reference compound. This method allows separation of the σ-donation and π-acceptor interactions of the ligand through ligand-to-metal and metal-to-ligand charge-transfer mixing pathways. The analysis shows that the {FeNO}6 electronic structure is best described as FeIII-NO(neutral), with no localized electron in an NO π* orbital or electron hole in an Fe dπ orbital. This delocalization comes from the large energy gap between the Fe-NO π-bonding and antibonding molecular orbitals relative to the exchange interactions between electrons in these orbitals. This study demonstrates the utility of L-edge XAS in experimentally defining highly delocalized electronic structures.

[1]  N. Lehnert,et al.  Heme-nitrosyls: electronic structure implications for function in biology. , 2015, Accounts of chemical research.

[2]  E. Alp,et al.  Comprehensive Fe–Ligand Vibration Identification in {FeNO}6 Hemes , 2014, Journal of the American Chemical Society.

[3]  K. Hodgson,et al.  Preparation of non-heme {FeNO}7 models of cysteine dioxygenase: sulfur versus nitrogen ligation and photorelease of nitric oxide. , 2013, Journal of the American Chemical Society.

[4]  P. Mascharak,et al.  Light-triggered nitric oxide delivery to malignant sites and infection , 2013, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[5]  K. Hodgson,et al.  Iron L-edge X-ray absorption spectroscopy of oxy-picket fence porphyrin: experimental insight into Fe-O2 bonding. , 2013, Journal of the American Chemical Society.

[6]  E. Solomon,et al.  Activation of α-keto acid-dependent dioxygenases: application of an {FeNO}7/{FeO2}8 methodology for characterizing the initial steps of O2 activation. , 2011, Journal of the American Chemical Society.

[7]  K. Hodgson,et al.  S K-edge X-ray absorption spectroscopy and density functional theory studies of high and low spin {FeNO}7 thiolate complexes: exchange stabilization of electron delocalization in {FeNO}7 and {FeO2}8. , 2011, Inorganic chemistry.

[8]  K. Hodgson,et al.  Fe L-edge X-ray absorption spectroscopy determination of differential orbital covalency of siderophore model compounds: electronic structure contributions to high stability constants. , 2010, Journal of the American Chemical Society.

[9]  K. Hodgson,et al.  Fe L- and K-edge XAS of low-spin ferric corrole: bonding and reactivity relative to low-spin ferric porphyrin. , 2009, Inorganic chemistry.

[10]  N. Lehnert,et al.  Electronic structure of six-coordinate iron(III)-porphyrin NO adducts: the elusive iron(III)-NO(radical) state and its influence on the properties of these complexes. , 2008, Journal of the American Chemical Society.

[11]  Sason Shaik,et al.  Nature of the Fe-O2 bonding in oxy-myoglobin: effect of the protein. , 2008, Journal of the American Chemical Society.

[12]  J. Lipscomb,et al.  VTVH-MCD and DFT studies of thiolate bonding to [FeNO]7/[FeO2]8 complexes of isopenicillin N synthase: substrate determination of oxidase versus oxygenase activity in nonheme Fe enzymes. , 2007, Journal of the American Chemical Society.

[13]  K. Hodgson,et al.  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. , 2007, Journal of the American Chemical Society.

[14]  K. Hodgson,et al.  Fe L-edge XAS studies of K4[Fe(CN)6] and K3[Fe(CN)6]: a direct probe of back-bonding. , 2006, Journal of the American Chemical Society.

[15]  P. Mascharak,et al.  Synthesis, structure, and properties of an Fe(II) carbonyl [(PaPy3)Fe(CO)](ClO4): insight into the reactivity of Fe(II)-CO and Fe(II)-NO moieties in non-heme iron chelates of N-donor ligands. , 2006, Inorganic chemistry.

[16]  K. Hodgson,et al.  Sulfur K-edge XAS and DFT calculations on nitrile hydratase: geometric and electronic structure of the non-heme iron active site. , 2006, Journal of the American Chemical Society.

[17]  P. Mascharak,et al.  Syntheses, structures, and reactivities of (Fe-NO)6 nitrosyls derived from polypyridine-carboxamide ligands: photoactive NO-donors and reagents for S-nitrosylation of alkyl thiols. , 2004, Inorganic chemistry.

[18]  K. Hodgson,et al.  L-edge X-ray absorption spectroscopy of non-heme iron sites: experimental determination of differential orbital covalency. , 2003, Journal of the American Chemical Society.

[19]  P. Mascharak,et al.  Iron nitrosyls of a pentadentate ligand containing a single carboxamide group: syntheses, structures, electronic properties, and photolability of NO. , 2003, Inorganic chemistry.

[20]  H. Shoun,et al.  Distribution, structure and function of fungal nitric oxide reductase P450nor—recent advances , 2002 .

[21]  K. Karlin,et al.  Nitric oxide in biological denitrification: Fe/Cu metalloenzyme and metal complex NO(x) redox chemistry. , 2002, Chemical reviews.

[22]  B. Fox,et al.  Mössbauer and EPR studies of the photoactivation of nitrile hydratase. , 2001, Biochemistry.

[23]  E. Dartyge,et al.  Photoinduced Ferrimagnetic Systems in Prussian Blue Analogues CIxCo4[Fe(CN)6]y (CI = Alkali Cation). 2. X-ray Absorption Spectroscopy of the Metastable State , 2000 .

[24]  A. Scuiller,et al.  SOFT X-RAY MAGNETIC CIRCULAR DICHROISM IN PARAMAGNETIC SYSTEMS : ELEMENT-SPECIFIC MAGNETIZATION OF TWO HEPTANUCLEAR CRIII MII6 HIGH-SPIN MOLECULES , 1999 .

[25]  B. Averill.  Dissimilatory Nitrite and Nitric Oxide Reductases. , 1996, Chemical reviews.

[26]  M. Verdaguer,et al.  Characterization of Chemical Bonds in Bimetallic Cyanides Using X-ray Absorption Spectroscopy at L2,3 Edges , 1996 .

[27]  A. Becke.  Density-functional thermochemistry. III. The role of exact exchange , 1993 .

[28]  G. Laan,et al.  The 2p absorption spectra of 3d transition metal compounds in tetrahedral and octahedral symmetry , 1992 .

[29]  R. D. Harcourt.  Comment on a CASSCF study of the FeO2 bond in a dioxygen heme complex , 1990 .

[30]  A. Becke,et al.  Density-functional exchange-energy approximation with correct asymptotic behavior. , 1988, Physical review. A, General physics.

[31]  Parr,et al.  Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. , 1988, Physical review. B, Condensed matter.

[32]  J. Perdew,et al.  Density-functional approximation for the correlation energy of the inhomogeneous electron gas. , 1986, Physical review. B, Condensed matter.

[33]  G. Sawatzky,et al.  3d x-ray-absorption lines and the 3d94fn+1 multiplets of the lanthanides. , 1985, Physical review. B, Condensed matter.

[34]  P. Butler.  Point Group Symmetry Applications: Methods and Tables , 1981 .

[35]  R. D. Cowan,et al.  The Theory of Atomic Structure and Spectra , 1981 .

[36]  Roald Hoffmann,et al.  Orbital interactions in metal dimer complexes , 1975 .

[37]  W. Goddard,et al.  Ozone model for bonding of an O2 to heme in oxyhemoglobin. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Enemark,et al.  Principles of structure, bonding, and reactivity for metal nitrosyl complexes , 1974 .

[39]  R. D. Harcourt.  Increased‐valence formulae and the bonding of oxygen to haemoglobin , 1971 .

[40]  L. Pauling,et al.  Nature of the Iron–Oxygen Bond in Oxyhæmoglobin , 1964, Nature.

[41]  JOSEPH J. WEISS,et al.  Nature of the Iron–Oxygen Bond in Oxyhæmoglobin , 1964, Nature.

[42]  C. D. Coryell,et al.  The Magnetic Properties and Structure of Hemoglobin, Oxyhemoglobin and Carbonmonoxyhemoglobin , 1936, Proceedings of the National Academy of Sciences.

[43]  A. Daiber,et al.  Nitric oxide reductase (P450nor) from Fusarium oxysporum. , 2005, Journal of inorganic biochemistry.

[44]  Frank M. F. de Groot,et al.  Multiplet effects in X-ray spectroscopy , 2005 .

[45]  Walker Fa.  Nitric oxide interaction with insect nitrophorins and thoughts on the electron configuration of the {FeNO}6 complex. , 2005 .

[46]  K. Hodgson,et al.  Spectroscopic and Theoretical Description of the Electronic Structure of S = 3/2 Iron-Nitrosyl Complexes and Their Relation to O2 Activation by Non-Heme Iron Enzyme Active Sites , 1995 .

[47]  I. Lindau,et al.  Atomic subshell photoionization cross sections and asymmetry parameters: 1 ⩽ Z ⩽ 103 , 1985 .

[48]  P. Butler.  Point Group Symmetry Applications , 1981 .

[49]  Donald S. McClure,et al.  Electronic Structure of Transition-Metal Complex Ions , 1960 .