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Title: Sulfur K-edge Spectroscopic Investigation of Second Coordination Sphere Effects in Oxomolybdenum-Thiolates: Relationship to Molybdenum-Cysteine Covalency and Electron Transfer in Sulfite Oxidase

Abstract

Second-coordination sphere effects such as hydrogen bonding and steric constraints that provide for specific geometric configurations play a critical role in tuning the electronic structure of metalloenzyme active sites and thus have a significant effect on their catalytic efficiency. Crystallographic characterization of vertebrate and plant sulfite oxidase (SO) suggests that an average O{sub oxo}-Mo-S{sub Cys}-C dihedral angle of {approx}77{sup o} exists at the active site of these enzymes. This angle is slightly more acute ({approx}72{sup o}) in the bacterial sulfite dehydrogenase (SDH) from Starkeya novella. Here we report the synthesis, crystallographic, and electronic structural characterization of Tp*MoO(mba) (where Tp* = (3,5-dimethyltrispyrazol-1-yl)borate; mba = 2-mercaptobenzyl alcohol), the first oxomolybdenum monothiolate to possess an O{sub ax}-Mo-S{sub thiolate}-C dihedral angle of {approx}90{sup o}. Sulfur X-ray absorption spectroscopy clearly shows that O{sub ax}-Mo-S{sub thiolate}-C dihedral angles near 90{sup o} effectively eliminate covalency contributions to the Mo(xy) redox orbital from the thiolate sulfur. Sulfur K-pre-edge X-ray absorption spectroscopy intensity ratios for the spin-allowed S(1s) {yields} S{sup v}(p) + Mo(xy) and S(1s) {yields} S{sup v}(p) + Mo(xz,yz) transitions have been calibrated by a direct comparison of theory with experiment to yield thiolate S{sup v}(p) orbital contributions, c{sup 2}{sub i}, to the Mo(xy) redox orbital and themore » Mo(xz,yz) orbital set. Furthermore, these intensity ratios are related to a second coordination sphere structural parameter, the O{sub oxo}-Mo-S{sub thiolate}-C dihedral angle. The relationship between Mo-S{sub thiolate} and Mo-S{sub dithiolene} covalency in oxomolydenum systems is discussed, particularly with respect to electron-transfer regeneration in SO.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL) National Synchrotron Light Source
Sponsoring Org.:
Doe - Office Of Science
OSTI Identifier:
930320
Report Number(s):
BNL-81030-2008-JA
Journal ID: ISSN 0020-1669; INOCAJ; TRN: US200822%%1468
DOE Contract Number:
DE-AC02-98CH10886
Resource Type:
Journal Article
Resource Relation:
Journal Name: Inorganic Chemistry; Journal Volume: 46; Journal Issue: 4
Country of Publication:
United States
Language:
English
Subject:
08 HYDROGEN; ABSORPTION SPECTROSCOPY; BONDING; COVALENCE; EFFICIENCY; ELECTRON TRANSFER; ELECTRONIC STRUCTURE; ENZYMES; HYDROGEN; OXIDASES; OXIDOREDUCTASES; PLANTS; REGENERATION; SPHERES; SULFITES; SULFUR; SYNTHESIS; TUNING; VERTEBRATES; YIELDS; national synchrotron light source

Citation Formats

Peariso,K., Helton, M., Duesler, E., Shadle, S., and Kirk, M. Sulfur K-edge Spectroscopic Investigation of Second Coordination Sphere Effects in Oxomolybdenum-Thiolates: Relationship to Molybdenum-Cysteine Covalency and Electron Transfer in Sulfite Oxidase. United States: N. p., 2007. Web. doi:10.1021/ic061150z.
Peariso,K., Helton, M., Duesler, E., Shadle, S., & Kirk, M. Sulfur K-edge Spectroscopic Investigation of Second Coordination Sphere Effects in Oxomolybdenum-Thiolates: Relationship to Molybdenum-Cysteine Covalency and Electron Transfer in Sulfite Oxidase. United States. doi:10.1021/ic061150z.
Peariso,K., Helton, M., Duesler, E., Shadle, S., and Kirk, M. Mon . "Sulfur K-edge Spectroscopic Investigation of Second Coordination Sphere Effects in Oxomolybdenum-Thiolates: Relationship to Molybdenum-Cysteine Covalency and Electron Transfer in Sulfite Oxidase". United States. doi:10.1021/ic061150z.
@article{osti_930320,
title = {Sulfur K-edge Spectroscopic Investigation of Second Coordination Sphere Effects in Oxomolybdenum-Thiolates: Relationship to Molybdenum-Cysteine Covalency and Electron Transfer in Sulfite Oxidase},
author = {Peariso,K. and Helton, M. and Duesler, E. and Shadle, S. and Kirk, M.},
abstractNote = {Second-coordination sphere effects such as hydrogen bonding and steric constraints that provide for specific geometric configurations play a critical role in tuning the electronic structure of metalloenzyme active sites and thus have a significant effect on their catalytic efficiency. Crystallographic characterization of vertebrate and plant sulfite oxidase (SO) suggests that an average O{sub oxo}-Mo-S{sub Cys}-C dihedral angle of {approx}77{sup o} exists at the active site of these enzymes. This angle is slightly more acute ({approx}72{sup o}) in the bacterial sulfite dehydrogenase (SDH) from Starkeya novella. Here we report the synthesis, crystallographic, and electronic structural characterization of Tp*MoO(mba) (where Tp* = (3,5-dimethyltrispyrazol-1-yl)borate; mba = 2-mercaptobenzyl alcohol), the first oxomolybdenum monothiolate to possess an O{sub ax}-Mo-S{sub thiolate}-C dihedral angle of {approx}90{sup o}. Sulfur X-ray absorption spectroscopy clearly shows that O{sub ax}-Mo-S{sub thiolate}-C dihedral angles near 90{sup o} effectively eliminate covalency contributions to the Mo(xy) redox orbital from the thiolate sulfur. Sulfur K-pre-edge X-ray absorption spectroscopy intensity ratios for the spin-allowed S(1s) {yields} S{sup v}(p) + Mo(xy) and S(1s) {yields} S{sup v}(p) + Mo(xz,yz) transitions have been calibrated by a direct comparison of theory with experiment to yield thiolate S{sup v}(p) orbital contributions, c{sup 2}{sub i}, to the Mo(xy) redox orbital and the Mo(xz,yz) orbital set. Furthermore, these intensity ratios are related to a second coordination sphere structural parameter, the O{sub oxo}-Mo-S{sub thiolate}-C dihedral angle. The relationship between Mo-S{sub thiolate} and Mo-S{sub dithiolene} covalency in oxomolydenum systems is discussed, particularly with respect to electron-transfer regeneration in SO.},
doi = {10.1021/ic061150z},
journal = {Inorganic Chemistry},
number = 4,
volume = 46,
place = {United States},
year = {Mon Jan 01 00:00:00 EST 2007},
month = {Mon Jan 01 00:00:00 EST 2007}
}
  • X-ray absorption spectra have been measured at the S K-, Cl K-, and Mo L{sub 3}- and L{sub 2}-edges for the d{sup 0} dioxomolybdenum(VI) complexes LMoO{sub 2}(SCH{sub 2}Ph), LMoO{sub 2}Cl, and LMoO{sub 2}(OPh) (L = hydrotris(3,5-dimethyl-1-pyrazolyl)borate) to investigate ligand-metal covalency and its effects on oxo transfer reactivity. Two dominant peaks are observed at the S K-edge (2,470.5 and 2,472.5 eV) for LMoO{sub 2}(SCH{sub 2}Ph) and at the Cl K-edge (2,821.9 and 2,824.2 eV) for LMoO{sub 2}Cl, demonstrating two major covalent contributions from S and Cl to the Mo d orbitals.Density functional calculations were performed on models of the three Momore » complexes, and the energies and characters of the Mo 4d orbitals were interpreted in terms of the effects of two strong cis-oxo bonds and additional perturbations due to the thiolate, chloride, or alkoxide ligand. The major perturbation effects are for thiolate and Cl{sup {minus}} {pi} mixed with the d{sub xz} orbital and {sigma} mixed with the d{sub z}{sup 2} orbital. The calculated 4d orbital energy splittings for models of these two major contributions to the bonding of thiolate and Cl ligands (2.47 and 2.71 eV, respectively) correspond to the splittings observed experimentally for the two dominant ligand K-edge peaks for LMoO{sub 2}(SCH{sub 2}Ph) and LMoO{sub 2}Cl (2.0 and 2.3 eV, respectively) after consideration of final state electronic relaxation. Quantification of the S and Cl covalencies in the d orbital manifold from the pre-edge intensity yields, {approximately} 42% and {approximately} 17% for LMoO{sub 2}(SCH{sub 2}Ph) and LMoO{sub 2}Cl, respectively. The Mo L{sub 2}-edge spectra provide a direct probe of metal 4 d character for the three Mo complexes. The spectra contain a strong, broad peak and two additional sharp peaks at higher energy, which are assigned to 2p transitions to the overlapping t{sub 2g} set and to the d{sub z}{sup 2} and d{sub xy} levels, respectively. The total peak intensities of the Mo L{sub 2}-edges for LMoO{sub 2}(OPh) and LMoO{sub 2}Cl are similar to and larger than those for LMoO{sub 2}(SCH{sub 2}Ph), which agrees with the calculated trend in ligand-metal covalency. The theoretical and experimental description of bonding developed from these studies provides insight into the relationship of electronic structure to the oxo transfer chemistry observed for the LMoO{sub 2}X complexes. These results imply that anisotropic covalency of the Mo-S{sub cys} bond in sulfite oxidase may promote preferential transfer of one of the oxo groups during catalysis.« less
  • In this communication, we explore the contributions of Cu-ligand and Cu-Cu bonding to valence delocalization and ET in the Cu{sub A} site of CcO. Sulfur K-edge X-ray absorption spectroscopy (XAS) provides the first direct experimental probe of copper-sulfur covalency in the half-occupied highest-energy molecular orbital (HOMO) of Cu{sub A} and two structurally-defined dithiolate-bridged models, delocalized mixed-valence 1 and dicupric 2. The Cu coordination environment of each system in shown in chart 1. Electronic absorption (Abs) and magnetic circular dichroism (MCD) spectroscopies are used to measure the total inter-ion electronic coupling in Cu{sub A} and 1 through identification of the classmore » III mixed-valence {Psi} {yields} {Psi}{sup *} transitions. The results from these techniques combine to define the pathways for delocalization in Cu{sub A} and 1 and to describe the individual Cu-S and Cu-Cu contributions to this process. The S K-edge data additionally reveal significant anisotropic Cu-ligand covalency, permitting comparison of competing N- and S-based ET pathways to and from the Cu{sub A} site. 20 refs., 2 figs.« less
  • No abstract prepared.
  • Sulfur K-edge X-ray absorption spectroscopy of a hydrogen-bonded elongated [Fe{sub 4}S{sub 4}]{sup 2+} cube is reported. The data show that this synthetic cube is less covalent than a normal compressed cube with no hydrogen bonding. DFT calculations reveal that the observed difference in electronic structure has significant contributions from both the cluster distortion and from hydrogen bonding. The elongated and compressed Fe{sub 4}S{sub 4} structures are found to have different spin topologies (i.e., orientation of the delocalized Fe{sub 2}S{sub 2} subclusters which are antiferromagnetically coupled to each other). It is suggested that the H-bonding interaction with the counterion does notmore » contribute to the cluster elongation. A magneto-structural correlation is developed for the Fe{sub 4}S{sub 4} cube that is used to identify the redoxactive Fe{sub 2}S{sub 2} subclusters in active sites of HiPIP and ferredoxin proteins involving these clusters.« less
  • X-ray absorption spectroscopy at the molybdenum and sulfur K-edges has been used to probe the active site of wild-type and cysteine 207 {yields} serine mutant human sulfite oxidases. We compare the active site structures in the Mo(VI) oxidation states: the wild-type enzyme possesses two Mo=O ligands at 1.71 A and three Mo-S ligands at 2.41 A. The mutant molybdenum site is a novel trioxo site with Mo=O bond lengths of 1.74 A, with two Mn-S ligands at 2.47 A. We conclude that cysteine 207 is a ligand of molybdenum in wild-type human sulfite oxidase, and that, in the mutant, themore » Mo is ligated to an extra oxo group rather than the hydroxyl of the substituent serine 207. 36 refs., 7 figs., 1 tab.« less