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J. Phys. Chem. B 2008, 112, 4770-4778
Electronic Structure of Transition Metal-Cysteine Complexes from X-ray Absorption Spectroscopy Bonnie O. Leung,† Farideh Jalilehvand,*,† and Robert K. Szilagyi*,‡ Department of Chemistry, UniVersity of Calgary, Calgary, Alberta, T2N 1N4, Canada, and Department of Chemistry and Biochemistry, Montana State UniVersity, Bozeman, Montana 59717 ReceiVed: October 10, 2007; In Final Form: December 18, 2007
The electronic structures of HgII, NiII, CrIII, and MoV complexes with cysteine were investigated by sulfur K-edge X-ray absorption near-edge structure (XANES) spectroscopy and density functional theory. The covalency in the metal-sulfur bond was determined by analyzing the intensities of the electric-dipole allowed pre-edge features appearing in the XANES spectra below the ionization threshold. Because of the welldefined structures of the selected cysteine complexes, the current work provides a reference set for further sulfur K-edge XAS studies of bioinorganic active sites with transition metal-sulfur bonds from cysteine residues as well as more complex coordination compounds with thiolate ligands.
Introduction The amino acid cysteine (H2Cys ) HSCH2CH(NH3+)COO-) manifests a rich coordination chemistry due to its high affinity for a variety of transition metal ions via its functional groups: carboxylate (-COO-), amine (-NH2), and thiol (-SH). The metal-sulfur bonds are especially important in physiological systems at active sites of metalloenzymes, where electron transfer, catalytic activation of small molecules, and atom transfer reactions occur.1 In many cases, the active sites of these metalloenzymes are currently under investigation to gain insights as to how their electronic and geometric structures determine their chemical reactivity.2 The metal-sulfur bond covalency, defined as the S 3p contribution in ligand-based molecular orbitals, can serve as a descriptor of the electronic structure.2 The metal-ligand orbitals that are experimentally probed by X-ray absorption near-edge structure (XANES) spectroscopy generally are the unoccupied, antibonding combinations of metal d and ligand p orbitals and thus represent the counterpart of the most important covalent bonding interactions. For example, earlier investigations into the blue copper protein and rubredoxin active sites3 ascertained that the high covalency of the Cu-S and Fe-S bonds, respectively, allows for rapid long-range electron transfer via its redox active molecular orbitals.4 The sulfur 3p character of the metal-sulfur bond can be directly determined by sulfur K-edge XANES spectroscopy.5 The spectral features that originate from the excitation of sulfur 1s core electrons (K-edge) into unoccupied molecular orbitals with 3p character have been used effectively to study transition metal complexes with sulfur ligands.2,5,6 Since the sulfur 1s electron excitations are localized on the absorbing sulfur atom and transitions from sulfur 1s to metal nd orbitals are electric dipole forbidden, pre-edge features in the energy range of the sulfur K-edge (2.4-2.9 keV) appear below the rising-edge or ionization threshold. These features are present when mixing occurs between sulfur 3p and unoccupied metal orbitals.2 The intensity of these pre-edge features thus corresponds directly to the sulfur 3p character and can be used to determine the † ‡
University of Calgary. Montana State University.
covalency of a metal-sulfur bond.2 Kohn-Sham orbitals from density functional theory (DFT) calculations provide further means for identifying these transitions by calculating energy differences between the ground and the core-hole excited states of the complex and correlating the intensities of pre-edge features to calculated orbital covalencies.2 The current work focuses on structurally characterized cysteine complexes with metal ions in different d orbital electronic configurations: HgII (5d10), NiII (3d8), CrIII (3d3), and MoV (4d1). The complexes selected for the given study have been characterized structurally and provide a demonstrative set of examples for investigating differences between late (Hg and Ni) and early (Cr) as well as 3d (Cr) versus 4d (Mo) transition metal thiolate complexes. Furthermore, most of these model complexes provide simple and straightforward references of spectral features for coordination compounds that are relevant to metal toxicity (Hg,7 Cr,8,9 and Ni10) and to metalloprotein active sites (Ni11 and Mo9). Experimental Procedures Sample Preparation. Cysteine (H2Cys ) HSCH2CH (NH3+)COO-), sodium ethanethiolate (Na+CH3CH2S-), and sodium thiosulfate (Na2S2O3) were purchased from SigmaAldrich and used without further recrystallization. The crystalline compounds K2[Ni(Cys)2]‚1.5H2O,12 Na[Cr(Cys)2]‚2H2O,13 Na2[Mo2O4(Cys)2]‚5H2O,14 and a fine precipitate of [Hg(HCys)2]15(where HCys denotes -SCH2CH(NH3+)COOand Cys denotes -SCH2CH(NH2)COO-) were synthesized as described previously. X-ray Absorption Spectroscopy. Sulfur K-edge XANES spectra of solid cysteine, 50 mM cysteine in an aqueous solution at pH 6.9 and 13, and solid Na[Cr(Cys)2]‚2H2O were collected at ambient temperature and atmospheric helium pressure at beamline 6-2, Stanford Synchrotron Radiation Laboratory (SSRL). The storage ring was operated under conditions of 3.0 GeV and 80-100 mA. A nickel coated mirror in the front of a Si(111) double crystal monochromator was used for harmonic rejection. For the solid [Hg(HCys)2], K2[Ni(Cys)2]‚1.5H2O, and Na2[Mo2O4(Cys)2]‚5H2O compounds, the spectra were collected under similar conditions using a nickel/rhodium coated mirror
10.1021/jp7098976 CCC: $40.75 © 2008 American Chemical Society Published on Web 03/20/2008
Structure of Transition Metal-Cysteine Complexes
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Figure 1. Structure of [HgII(HCys)2] precipitate (anti conformation, DFT optimized geometry) (1) and crystalline K2[NiII(Cys)2] (2), Na[CrIII (Cys)2] (3), and Na2[MoV2O4(Cys)2] (4) (refs 12-14).
for harmonic rejection at beamline 9-A of the Photon Factory (PF), High-Energy Accelerator Research Organization (Tsukuba, Japan), operating at 2.5 GeV and 250-300 mA. The spectrum of the sodium ethanethiolate salt was obtained at beamline 9.3.1 of the Advanced Light Source (ALS) under ultrahigh vacuum (10-7 Torr), using a liquid nitrogen cooled sample rod and a nickel coated harmonic rejection mirror under ring conditions of 1.9 GeV and 250-500 mA. The solid samples were ground finely and dusted on sulfurfree Mylar tape. All data at SSRL and PF were collected in fluorescence mode with a nitrogen-filled Lytle detector (I1) and a helium-filled ion chamber (I0) that was placed before the sample chamber. Fluorescence data (I1) at ALS were obtained by a Si-photodiode (Hamamatsu), and the incident beam intensity (I0) was measured by aluminized Mylar tape. The repeated scans of 3-8 were averaged with the program suite EXAFSPAK16 after externally calibrating the energy scale by assigning the first peak maximum in the S K-edge XANES spectrum of Na2S2O3‚5H2O to 2472.02 eV.2 The resulting spectra were background subtracted with a first-order polynomial and normalized above the edge jump at 2490 eV. Computational Details. Crystallographic atomic coordinates of cysteine, K2[Ni(Cys)2]‚1.5H2O, Na[Cr(Cys)2]‚2H2O, and Na2[Mo2O4(Cys)2]‚5H2O were obtained from the Cambridge Structural Database (CSD)17 (see Figure 1) and were slightly adjusted to achieve C2 symmetry for the [Ni(Cys)2]2- and [Mo2O4(Cys)2]2complexes, while the Na[Cr(Cys)2] structure was used without symmetry constraints. All coordinates are provided as Supporting Information (Tables S1a-S1d). To evaluate the effect of counterions, a neutralizing field of point charges was employed for the K2[Ni(Cys)2]‚1.5H2O system. The atomic coordinates of the deprotonated cysteine (Cys2-) ligand and the [Hg(HCys)2] complex were obtained from geometry optimizations using the Amsterdam Density Functional (ADF) package.18-20 The Hg-S bond distance was previously determined by extended X-ray absorption fine structure (EXAFS) spectroscopy to be 2.34 Å.15 Both the cis and the trans conformations of the [Hg(HCys)2] complex were evaluated with C2 symmetry and were found to
give similar results. Here, we report results on the trans configuration. All ground and excited state DFT calculations were performed using the ADF program employing triple-ζ basis sets extended with two polarization functions for the ligand (TZ2P) and polarization with diffuse functions for NiII and CrIII (TZ2P+). Triple-ζ small frozen core basis sets with polarization functions (TZP) were used for HgII and MoV. The density functional exchange and correlation interactions were described by the Slater-type local exchange21,22 and Vosko-Wilk-Nusair local correlation23 approximation extended with the Becke24 and Perdew25 generalized gradient approximation (GGA) functionals. Solvation effects for the cysteine solutions (i.e., the zwitterion (H2Cys ) HSCH2CH(NH3+)COO-) at pH 6.9 and the fully deprotonated cysteinate ion (Cys2-) at pH 13) were simulated using the Conductor-like Screening Model (COSMO) method.26 For water, a dielectric constant of 78.5 was used. Mulliken population analysis (MPA),27 Hirschfeldt charge analysis (HCA),28,29 and Voronoi deformation density calculations (VDD)30,31 were used to determine the spin densities and atomic charges. Spectral Features and Ligand Covalency. To determine the number of main transitions in the XANES region of the sulfur K-edge spectra, the pre-edge features were fitted with pseudoVoigt lines using the EDG_FIT program within EXAFSPAK.16 Pseudo-Voigt lines approximated with a 1:1 Gaussian/Lorentzian line-shape combination previously were found to be suitable for pre-edge quantitation.32,33 The area of the appropriate preedge feature can be used to quantify the covalency of the metalsulfur bond by means of eq 1:2
D0 ) (1/3n)R2I(thiolate S 1s f S 3p)
(1)
where D0 is the total experimental intensity estimated by the product of twice of the half-height line width (eV) and the peak height/intensity, n is the normalization factor related to the number of absorbers, R2 is the covalency or ligand character in the metal-ligand bonding interactions, and I(thiolate S 1s f S 3p) is the dipole integral for the S 1s f S 3p transition that
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Figure 2. Sulfur K-edge XANES spectra (A) of (a) 50 mM cysteine solution at pH ) 6.9, (b) solid cysteine, (c) solid sodium ethanethiolate, and (d) 50 mM cysteine solutions at pH 13 with corresponding smoothed second derivative (B).
previously for thiolate ligands was determined to be 8.05 eV from the active site of the blue Cu protein and their biomimetic models.5 We used both the second derivatives and the molecular orbitals from electronic structure calculations to determine the lowest number of features needed for fitting. As rising-edge features tend to be less resolved due to the low-energy tail of the edge jump and overlap from atomic scattering, the fits of well-separated pre-edge features are of higher accuracy and reliability. Results and Discussion Qualitative Comparison of Free Thiol Ligands. The sulfur K-edge spectra of solid cysteine, sodium ethanethiolate, and two cysteine solutions at pH 6.9 and 13 are presented in Figure 2. The spectra of solid cysteine (Figure 2b) and the 50 mM cysteine solution at pH 6.9 (Figure 2a) display similar energies for the main peak, which is slightly more intense for the cysteine solution because of the reduced self-absorption of the fluorescence signal. Similar spectra previously have been qualitatively interpreted by Pickering et al., with the main feature at 2473.4 eV assigned to the S 1s f C-S σ* transition.34 The cysteinate (Cys2-) solution at pH 13 shows a shift in the S 1s f C-S σ* transition to a lower energy by 1.1 eV (2472.3 eV). The shift is mainly due to the negative charge of the thiolate (RS-) group. The penetration of sulfur 3p electrons increases the shielding of the sulfur nuclear charge for sulfur 1s more for a negatively charged thiolate than in the protonated thiol, which raises the energy of the sulfur 1s orbital and thus decreases the energy gap between the 1s and the C-S σ* orbitals in the thiolate sulfur. Sodium ethanethiolate provides a model for deprotonated cysteine, where the effect of the absence of the amino (NH3+) and carboxylate (COO-) functional groups on spectral features also can be directly evaluated. The position of the main peak in the S K-edge XANES spectrum of the CH3CH2S- ion occurs at 2472.1 eV, which is slightly lower than that of Cys2- at pH
TABLE 1: Population Analysis for Solid Cysteine, Sodium Ethanethiolate, and Cysteine Solutions at pH 6.9 and 13 Comparing Population Analysis Methods MPA, HCA, and VDD solids
MPA HCA VDD
solutions
cysteine
sodium ethanethiolate
cysteine (pH 6.9)
cysteine (pH 13)
-0.008 -0.058 -0.131
-0.804 -0.672 -0.703
-0.059 -0.059 -0.147
-0.783 -0.570 -0.602
13 (2472.3 eV). The beamline resolution and reproducibility is 0.1 eV. This energy change can be correlated with the negative inductive effects of the amine and carboxylate functional groups that pull electron density away from the thiol sulfur atom in Cys2-, thus making it more positive and shifting the transition to a higher energy. This interpretation assumes about the same magnitude of environmental effect from the hydrated thiolate in solution and the sodium point charge surrounded thiolate in the solid phase. For testing that assumption, we carried out electronic structure calculations with various solvated models. DFT Calculations of Cysteine. Geometry optimizations by DFT calculations using the COSMO solvation model were performed for the thiols and the thiolate species. The charge distribution was analyzed by various population analysis methods (Table 1). For cysteine in the solid state and in solution at pH 6.9, the formal charge of the sulfur atom within the sulfhydryl group is zero, which corresponds to calculated atomic charges of about -0.06 to -0.15 e- (see Table 1). The population analyses for the ethanethiolate ion and the Cys2ion in aqueous solution at pH 13 result in considerably more negative atomic charges of -0.57 to -0.80 e- as expected. The sulfur charges obtained for the Cys2- ion in solution are slightly more positive than for the CH3CH2S- ion (-0.78 -to -0.60 e- vs -0.80 -to -0.70 e-), which is indicative of the previously mentioned electron withdrawing nature of the amino and
Structure of Transition Metal-Cysteine Complexes SCHEME 1: Models Employed To Analyze the Solvent Effect
carboxylate functional groups, giving good agreement with the differences in the spectral features. DFT Analysis of Solvent Effects. The cysteine molecule and cysteinate ion provide an opportunity to compare theoretical solvent models in four approaches: gas-phase calculations for reference, COSMO continuum model, explicit solvent molecules, and the latter two combined (Scheme 1 A-D). The experimental energy difference between the S 1s f C-S σ* excitation for the cysteine solutions at pH 6.9 and 13 is 1.1 eV. The relative orbital energies obtained from gas-phase calculations underestimate this value by 0.5 eV. Implementation of the COSMO continuum provides a relative energy difference of 1.0 eV. Seven explicit water molecules were added to the cysteine species, and their positions were optimized. The obtained relative energy of 1.2 eV slightly overestimates the experimental value. The final model combined both the explicit water molecules with the COSMO solvation continuum and resulted in a relative energy of 1.1 eV, an exact match to the experimental data. The comparison of the previous four approaches suggests that either the COSMO solvation method or the explicit solvent molecules can account for most of the solvent effects on the ground state molecular orbital energy levels, but preferably, both should be applied if the size of the computational model does not make it prohibitive. Qualitative Comparison of Metal-Cysteine Complexes. The sulfur K-edge XANES spectra of the investigated metalcysteine complexes are shown in Figure 3. The spectrum of the [Hg(HCys)2] complex displays two rising-edge transitions at 2472.3 and 2473.1 eV. Since the d-manifold is fully occupied for the d10 mercury(II) ion, no pre-edge features are observed below the rising-edge. For the K2[Ni(Cys)2], Na[Cr(Cys)2], and [Mo2O4(Cys)2]2complexes, the spectra show distinct pre-edge transitions at lower energies (i.e., 2471.1, 2471.3, and 2471.7 eV), respectively. The second derivatives of these spectra display a sharp minimum for K2[Ni(Cys)2]; however, for both Na[Cr(Cys)2] and Na2[Mo2O4(Cys)2], the less resolved and broader pre-edge features suggest the presence of envelopes of transitions (see Figure 3B). The energies of the pre-edge features increase in the order CrIII (3d3) ≈ NiII (3d8) < MoV (4d1). Previous studies have
J. Phys. Chem. B, Vol. 112, No. 15, 2008 4773 shown that as the effective nuclear charge increases on the metal ion, the stabilization of the d orbitals results in lower transition energies in the sulfur XANES.35 This trend was observed for highly similar coordination environments, while the current study encompasses transition metal complexes in both different oxidation states and coordination environments. To understand the origin of the pre-edge energy positions and intensities for the given set of compounds, the metal charge, the number of electron holes in the valence d orbitals, the coordination environment, and the ligand field splitting need to be simultaneously considered. DFT, which is useful to follow changes in the electronic structure,2 was employed to model the electronic structure contributions to the position and intensity of the preedge features and the main peaks. Analysis of the d10 Mercury(II) Complex. The spectrum of the [Hg(HCys)2] complex was fitted with peaks that slightly deviate from the ideal pseudo-Voigt lines36 (with Gaussian/ Lorentzian ratios between 0.37 and 0.52 eV and line widths of 0.55-0.77 eV) due to the transition envelope nature of the rising-edge features (Figure 4 and Table S2). On the basis of the second derivative spectra, the resolved three transition envelopes are separated from each other by approximately 0.9 eV (2472.1, 2473.0, and 2473.9 eV) with the edge position at approximately 2473.9 eV. DFT analysis of the ground state shows transitions with significant mixing of sulfur 3p character, corresponding to S 1s f Hg 6s (LUMO), S 1s f Hg 6p (LUMO + 2, peak 1), S 1s f C-S σ* (peak 2, LUMO + 5), and S 1s f S 4p (peak 3) transitions, respectively (see Table 2 and Figure 8). The first two transitions become electric dipole allowed due to the mixing of the sulfur 3p with Hg 6s and 6p orbitals. Transitions to unoccupied antibonding orbitals reflect the sulfur 3p covalency of the bonding orbitals with Hg s and p characters and the C-S σ* orbital, as well as the sulfur Rydberg orbitals with sulfur 4p character. Because of the lack of a transition dipole integral for 4p-based transitions, Table 2 only lists the transitions that have considerable sulfur 3p character. The presence of LUMO and LUMO + 2 orbitals is consistent with the valence bond picture of an sp hybridized HgII ion binding to two thiolates. The S 1s f C-S σ* transitions are assigned to 2473.0 eV for the HgII complex and are also present for all other complexes. The position of this transition appears at 0.3 eV lower for the Ni (2472.7 eV) and Cr (2472.7 eV) complexes. Since the C-S bond lengths are within 1.80-1.85 Å for each studied complex, this energy position can be used as a reference to compare the relative sulfur effective nuclear charge among the complexes. Changes in the energy of the C-S σ* orbital are directly affected by a shift in the 1s core level, with the energy of the main peak shifting lower for a more negatively charged ligand. The use of the C-S σ*-based transitions as a reference is generally preferred due to its more resolved nature relative to the S 4p-based transitions. As shown in Table 2, the relative energy difference of the calculated transitions match reasonably well with the experimental values. The intensities of the deconvoluted transitions in the sulfur XANES spectrum correspond to the sulfur covalency contribution to the bonds, indicating 17% sulfur 3p character in the Hg 6s and one of the 6p orbitals and 31% S 3p character in the C-S σ* orbital. The S 4p character in peak 3 could not be quantified due to the lack of transition dipole integral for S 4p transitions. Slightly higher sulfur contributions were obtained from DFT calculations than from experiment by peak-fitting, which is consistent with previous observations that gradient corrected density functionals can overestimate the ligand covalency of metal-ligand bonds.6,37
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Figure 3. Sulfur K-edge XANES spectra of [Hg(HCys)2], K2[Ni(Cys)2]‚1.5H2O, Na[Cr(Cys)2]‚2H2O, and Na2[Mo2O4(Cys)2]‚5H2O (A) with corresponding smoothed second derivative (B). (Spectra from ref 40.)
Figure 4. Representative fits of the sulfur K-edge XANES region of [Hg(HCys)2] (linewidths, peak positions, and intensities are given in Table S2) (in the Y axis, numbers are partially covered).
Analysis of the d8 Nickel(II) Complex. Fitting of the spectral features of the K2[Ni(Cys)2] sample reveals a well-resolved preedge feature at 2471.1 eV (peak 1), followed by a main feature (peak 2) at 2472.7 eV (peak 3) (Figure 5) and an additional feature at 2474.2 eV. These peaks can be assigned to excitations of sulfur 1s core electrons to NiII 3dxy-S antibonding (LUMO), C-S σ* (LUMO + 3 in Figure 8), and S 4p-based Rydberg orbitals. The area for the pre-edge transition (peak 1) corresponds to a total sulfur 3p character of 45%. With two electron holes in the d manifold of Ni2+, this corresponds to a covalency of 22.5% sulfur 3p character in the Ni dxy orbital per electron hole (Tables 2 and S2). Similarly, the total area under peak 2 corresponds to two electron holes in the C-S σ* orbital with 35% sulfur 3p character per electron hole.
The calculated electronic structure for the nickel complex was further investigated by comparing two models for the charge neutralization of the [Ni(Cys)2]2- complex. The first model used two potassium atoms from the crystal structure to obtain an overall neutral charge, while the second model used a symmetrical distribution of positive point charges. The orbital compositions did not vary by more than 5%; however, the absolute energies of the orbitals were significantly different. With the model containing asymmetrically placed potassium atoms, the relative energy between the first two transitions was 2.9 eV, with symmetrical point charges of 1.7 eV, which is in better agreement with the experimental value of 1.6 eV. Analysis of the energy diagram of the d orbitals obtained from DFT calculations using a neutralizing field of negative charges indicates that the pre-edge peak corresponds to the
Structure of Transition Metal-Cysteine Complexes
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Figure 5. Representative fits of the sulfur K-edge XANES region of K2[Ni(Cys)2] using pseudo-Voigt lines (linewidths, peak positions, and intensities are given in Table S2).
TABLE 2: Comparison of Experimental and Calculated Pre-edge Transition Energies and Intensities for XAS Spectra of Cysteine Metal Complexesa relative energies (eV) complex [Hg(HCys)2]
transition S 1s f
electron holes
exptl
calcd
exptl
calcd
1
Hg 6s Hg 6p C-S σ* Ni 3dxy C-S σ* Cr 3dyz (β) Cr dx2-y2(Rβ) Cr dz2 (Rβ) C-S σ* Mo dx2-y2 Mo dz2 C-S σ*
2 2 2 2 2 1 2 2 2 2 2 2
0.0
0.0
17
0.9 0.0 1.6 0.0
0.7 0.0 0.7 0.0 0.4 0.3 1.1 0.0 0.6 1.2
31 23 35 39b
26 6 44 33 36 34 18 24 39 30 21 18
[Cr(Cys)2]+
2 1 2 1
[Mo2O4(Cys)2]2-
2 1
[Ni(Cys)2]2+
S 3p % per hole
peak
2
1.5 0.0 1.5
49 37b 63
a
Sulfur 3p covalency values were obtained from using eq 1. See Figures 4-7 and Table S2 for experimental results. Note that the S 1s f 4p transitions are not listed here. b Total S 3p character.
transitions S 1s f Ni 3dxy with 33% S 3p character per electron hole, followed by the S 1s f C-S σ* as the most intense feature (LUMO and LUMO + 3, respectively, in Figure 8). As found for the mercury complex, the GGA DFT seems to overestimate the covalency of the Ni-S bonds as well. In the previously characterized tetrahedral d8 tetrathiolatonickel(II) complex,5,38 the pre-edge peak for [Ni(S-2-PhC6H4)4]2- occurred at a lower energy (2470.5 eV) than for K2[Ni(Cys)2] (2471.1 eV). This is likely due to differences in the ligand field splitting and spin states between the tetrahedral and the tetragonal complex in the triplet and singlet ground states, respectively, as well as the difference in metal-ligand covalency reflected by the different pre-edge intensities (Figure S1). The covalency of the NiII-S bond was determined for [Ni(S-2-Ph-C6H4)4]2- to be 17% per electron hole from four thiolate sulfurs,5 while for K2[Ni(Cys)2], the Ni-S covalency was 23% per electron hole from two thiolate sulfurs (Table 2). This can be rationalized by the thiolate ligands being able to donate more electrons in the cysteine complex, due to the increased orbital overlap in square planar geometry (Ni-S is 2.199-2.208 Å) than in the axially compressed tetrahedral complex with a Ni-S distance of 2.288(2) Å.7,38 Analysis of the d3 Chromium(III) System. As expected from the presence of an increased number of electron holes in CrIII relative to NiII complexes, a broad pre-edge feature was
observed for the [Cr(Cys)2]- complex at 2471.2 eV. This was fitted by a non-Voigt line transition envelope of a Gaussian/ Lorentzian ratio of 0.59 and a linewidth of 0.58 eV (Table 2). This envelope can be related to transitions to the t2g and eg orbitals of an approximately octahedral coordination environment (see Figures 1 and 8). As for the other thiolate complexes, the most intense peak at 2472.7 eV corresponds to the S 1s f C-S σ* transition and is fitted with an envelope of transitions. The area under the pre-edge feature corresponds to 39% of total sulfur 3p character for the entire pre-edge feature (Table 2). The ground state of the d3 [Cr(Cys)2]- complex was calculated to be a quartet state (S ) 3/2), which is about 0.9 eV more stable than the doublet state. In these calculations, we considered a sodium counterion at its crystallographic positions. With a d3 valence electron configuration, excitations of the sulfur 1s electron to seven molecular orbitals are possible. However, due to the coordination geometry of the thiolate ligands, sulfur 3p mixing occurs only with Cr dz2, dx2-y2 (eg-type for σ-bonding, RLUMO, RLUMO + 1, βLUMO + 5, and βLUMO + 6), and dxz (t2g-type for π-bonding and βLUMO + 2) orbitals (Figure 8). Note that due to the presence of unpaired electrons on the Cr center, there is a slight difference between the spin-up (R) and spin-down (β) orbitals; however, the overall metal-ligand bonding is the same for RLUMO and βLUMO + 5, as well as for RLUMO + 1 and βLUMO + 6. As observed previously
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Figure 6. Representative fits of the sulfur K-edge XANES region of Na[Cr(Cys)2] using pseudo-Voigt lines (linewidths, peak positions, and intensities are given in Table S2).
Figure 7. Representative fits of the sulfur K-edge XANES region of [Mo2O4(Cys)2]2- using pseudo-Voigt lines (linewidths, peak positions, and intensities are given in Table S2).
for other complexes, the calculated orbital covalencies are slightly overestimated (Table 2). Note that the underestimated S 3p character of the C-S σ* orbital is more likely due to the difficulty of extracting quantitative information from higher energy rising features where signals from bound excited states begin to mix with features from atomic scattering. Analysis of the d1 Dinuclear Molybdenum(V) System. In a similar way as for the CrIII complex, the broad pre-edge XANES feature at 2471.6 eV for Na2[Mo2O4(Cys)2] in Figure 3 suggests that there are several transitions in this region. The greatest deviation from the pseudo-Voigt line (0.71) and the wide linewidth (0.56 eV) further supports this conclusion. The peak-fitting procedure resulted in an integrated area for the envelope that corresponds to 37% S 3p covalency (Figure 7 and Table S2). The Na2[Mo2O4(Cys)2] complex is diamagnetic.39 The unpaired electron on each Mo center was evaluated by considering both singlet states (a closed shell covalent and open shell localized bi-radical) as well as a triplet state (2S + 1 ) 3), and it was found that the closed shell diamagnetic complex has the
lowest energy by 1.6 eV relative to the triplet state. The open shell localized bi-radical electronic structure converged to the delocalized diamagnetic structure. The experimentally probed molecular orbitals for [Mo2 O4(Cys)2]2- are shown in Figure 8. The calculated molecular orbitals for the [Mo2O4(Cys)2]2- system shows a negligible sulfur 3p contribution for the dxz and dyz orbitals since the sulfur atoms are in the xy plane. This means that the thiolate ligands act dominantly as σ-donor ligands. Their π-donor ability is repressed by the strong π-donor bridging oxo ligands. The two molecular orbitals that give rise to the major preedge features are LUMO + 9 and LUMO + 10. They were calculated to contain 30 and 19% S 3p contributions. The comparison of experimental and theoretical values of the covalency and energy positions parallels the other three studied complexes. Conclusion The peak energies and intensities of sulfur K-edge XANES spectral features of the crystalline metal-cysteine complexes
Structure of Transition Metal-Cysteine Complexes
J. Phys. Chem. B, Vol. 112, No. 15, 2008 4777 and thus decreases the energy gap between the sulfur 1s and C-S σ* orbitals. The energy of this transition follows the trend cysteine H2Cys pH 6.9 (2473.4 eV) > [HgII(HCys)2] (2473.1 eV) ) Na2[MoV2O4(Cys)2] (2473.1 eV) > K2[NiII(Cys)2] (2472.9 eV) g Na[CrIII(Cys)2] (2472.8 eV) > cysteinate Cys2pH 13.0 (2472.3 eV). Thus, specific transitions in the sulfur K-edge XANES spectra of cysteine as a ligand to transition metal ion can yield detailed electronic information about the character of the metal-sulfur bonds. The pre-edge features were found to be quite sensitive to the coordination and bonding to the sulfur atom. This work provides some references with respect to spectral features, their assignments, and electronic structure characterizations for coordination compounds relevant to Hg, Cr, and Ni toxicity as well as bioinorganic active sites. Acknowledgment. This work was financially supported by the Natural Sciences and Engineering Council (NSERC) of Canada, the Canadian Foundation for Innovations (CFI), and the Province of Alberta (ASRIP). The X-ray absorption spectra were measured at the Stanford Synchrotron Radiation Laboratory (SSRL Proposal 2848) and the Photon Factory, Tsukuba, Japan (Proposal 2003G286). The SSRL Structural Molecular Biology Program is supported by the Department of Energy, Office of Biological and Environmental Research and by the National Institutes of Health, National Center for Research Resources, Biomedical Technology Program. R.K.S. acknowledges funding from the MSU Center of Bio-Inspired Nanomaterials (ONR N00014-06-01-1016). F.J. is recipient of NSERC University Faculty Award (UFA). Supporting Information Available: Normalized XANES spectra of [Ni(S-2-Ph-C6H4)4]2- from ref 5, coordinates of computational models, and summary of fitting parameters. This information is available free of charge via the Internet at http:// pubs.acs.org.
Figure 8. Molecular orbital energy plots of the experimentally probed orbitals with significant sulfur 3p character.
References and Notes
[Hg(HCys)2], K2[Ni(Cys)2]‚1.5H2O, Na[Cr(Cys)2]‚2H2O, and Na2[Mo2O4(Cys)2]‚5H2O are distinctly different. The welldefined low-energy pre-edge feature in the spectrum of the NiII complex broadens for CrIII and MoV and disappears for the HgII complex. The DFT method employed allows for the assignment and quantitative analysis of such characteristic pre-edge features that appear for these transition metal-cysteine complexes. The energy of the pre-edge feature, which corresponds to the S 1s f metal d orbital transition, increases as the effective nuclear charge of the metal ion decreases, in the order CrIII (3d3) ≈ NiII (3d8) < MoV (4d1). The covalency of the transition metal-sulfur bonds was estimated from the resolved pre-edge features. The intensity of the pre-edge feature does not always follow a linear trend versus total covalency, due to the complexity of the origin of the preedge features. The total sulfur covalencies were determined by XAS measurements (and DFT calculations) to be 45% (66%) for K2[Ni(Cys)2], 39% (55%) for Na[Cr(Cys)2], and 37% (102%) for Na2[Mo2O4(Cys)2]. The rising-edge feature in the XANES spectra of these transition metal- cysteine complexes corresponds to the S 1s f C-S σ* transition, and its energy position approximates the nuclear charge of the sulfur absorber. As the negative charge on the sulfur atom increases, the rising-edge feature shifts to lower energy because the shielding of the nuclear charge increases more for the sulfur 1s orbital than for the 3p orbitals
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