Influence of the ligand-field on EPR parameters of cis- and trans-isomers in MoV systems relevant to molybdenum enzymes: Experimental and density functional theory study

Abstract

The electron paramagnetic resonance (EPR) investigation of mononuclear cis- and trans-(L1O)MoOCl₂ complexes [L1OH = bis(3,5-dimethylpyrazolyl)-3-tert-butyl-2-hydroxy-5-methylphenyl)methane] reveals a significant difference in their spin Hamiltonian parameters which reflect different equatorial and axial ligand fields created by the heteroscorpionate donor atoms. Density functional theory (DFT) was used to calculate the values of principal components and relative orientations of the g and A tensors, and the molecular framework in four pairs of isomeric mononuclear oxo‑molybdenum(V) complexes (cis- and trans-(L1O)MoOCl₂, cis,cis- and cis,trans-(L-N₂S₂)MoOCl [L-N₂S₂H₂ = N,N'-dimethyl-N,N'-bis(mercaptophenyl)ethylenediamine], cis,cis- and cis,trans-(L-N₂S₂)MoO(SCN), and cis- and trans-[(dt)₂MoO(OMe)]^2- [dtH₂ = 2,3-dimercapto-2-butene]). Scalar relativistic DFT calculations were conducted using three different exchange-correlation functionals. It was found that the use of hybrid exchange-correlation functional with 25% of the Hartree-Fock exchange leads to the best quantitative agreement between theory and experiment. A simplified ligand-field approach was used to analyze the influence of the ligand fields in all cis- and trans-isomers on energies and contributions of molybdenum d-orbital manifold to g and A tensors and relative orientations. Specifically, contributions that originated from the spin-orbit coupling of the d_xz, d_yz, and d_x2-y2 orbitals into the ground state have been discussed. The new findings are discussed in the context of the experimental data of mononuclear molybdoenzyme, DMSO reductase.

Keywords: DFT calculations; DMSO reductase; EPR spectroscopy; Molybdenum enzymes; Molybdenum hyperfine parameters.

Figure 1.

Top: Schematic representation of molybdenum cofactor (Moco) that can exist in pyran ring close and open forms. In some enzymes, the phosphate group is replaced by dinucleotide. Bottom: Schematic representation of the active sites of three Moco containing enzyme families shown in basic form. Significant diversity within the family exists and for more details, see reference .

Figure 2.

The isomeric complexes used in this investigation.

Figure 3.

X-band EPR spectrum (red line) and simulation (black line) of cis-(L1O)MoOCl₂ in 50:50 toluene:chloroform. Experimental conditions: microwaves, 0.02 mW at 9.621GHz; temperature, 15 K. Simulation parameters: $\mathrm{g}=\left(\mathrm{1.929,1.941,1.945}\right)$; $\mathrm{A}=\left(\mathrm{105,96,226}\right)\mathrm{M}\mathrm{H}\mathrm{z}$; ${\mathrm{\alpha }}_{\mathrm{x}\mathrm{y}},={20}^{°}$, ${\mathrm{\beta }}_{\mathrm{x}\mathrm{z}}={37}^{°}$.

Figure 4.

X-band EPR spectrum (red line) and simulation (black line) of trans-(L1O)MoOCl₂ in 50:50 toluene:chloroform. Experimental conditions: microwaves, 0.02 mW at 9.622GHz; temperature, 15 K. Simulation parameters: g = (1.946, 1.957, 1.965); A = (104, 90, 226) MHz; β_xz = 35°.

Figure 5.

DFT-predicted molecular orbital diagram of cis- and trans- (L1O)MoOCl². Occupied and unoccupied MOs are separated by horizontal dashed line, while the vertical dashed lines represent the change in the energy between $\mathrm{\alpha }$ and $\mathrm{\beta }$ orbitals.

Figure 6.

DFT-predicted molecular orbital diagram of cis,cis- and cis,trans-(L-N₂S₂)MoOCl. Occupied and unoccupied MOs are separated by horizontal dashed line, while the vertical dashed lines represent the change in the energy between $\mathrm{\alpha }$ and $\mathrm{\beta }$ orbitals.

Figure 7.

DFT-predicted molecular orbital diagram of cis,cis- and cis,trans-(L-N₂S₂)MoO(NCS). Occupied and unoccupied MOs are separated by horizontal dashed line, while the vertical dashed lines represent the change in the energy between $\mathrm{\alpha }$ and $\mathrm{\beta }$ orbitals.

Figure 8.

DFT-predicted molecular orbital diagram of cis- and trans-(dt)₂MoO(OMe). Occupied and unoccupied MOs are separated by horizontal dashed line, while the vertical dashed lines represent the change in the energy between $\mathrm{\alpha }$ and $\mathrm{\beta }$ orbitals.

Figure 9.

Frontier molecular orbital composition (in %) of cis- and trans-(L1O)MoOCl₂. Mo – green; O – red; Cl – blue; L1O – yellow

Figure 10.

Frontier molecular orbital composition (in %) of cis,cis- and cis,trans-(L-N₂S₂)MoOCl. Mo – green; O – red; Cl – blue; L-N₂S₂ – yellow.

Figure 11.

Frontier molecular orbital composition (in %) of cis,cis- and cis,trans-(L-N₂S₂)MoO(NCS). Mo – green; O – red; NCS – blue; L-N₂S₂ – yellow.

Figure 12.

Frontier molecular orbital composition (in %) of cis-(dt)₂MoO(OMe). Mo – green; O – red; (dt)eq/eq – blue; dt(eq/ax) – magenta; OMe – yellow, eq – equatorial, and ax, axial.

Figure 13.

(Left) Comparison of the calculated and experimental g-values. The linear correlation follows the equation, g(exp) = (0.86±0.06) g(dft) + 0.30 (±0.13) (R² = 0.91); (Right) Comparison of the calculated and experimental A-values. The linear correlation follows the equation, A(exp) = (1.15 ± 0.07) A(dft) − 7.55(± 8.92)(R² = 0.97)