Vibrational Control of Covalency Effects Related to the Active Sites of Molybdenum Enzymes

Abstract

A multitechnique spectroscopic and theoretical study of the Cp₂M(benzenedithiolato) (M = Ti, V, Mo; Cp = η⁵-C₅H₅) series provides deep insight into dithiolene electronic structure contributions to electron transfer reactivity and reduction potential modulation in pyranopterin molybdenum enzymes. This work explains the magnitude of the dithiolene folding distortion and the concomitant changes in metal-ligand covalency that are sensitive to electronic structure changes as a function of d-electron occupancy in the redox orbital. It is shown that the large fold angle differences correlate with covalency, and the fold angle distortion is due to a pseudo-Jahn-Teller (PJT) effect. The PJT effect in these and related transition metal dithiolene systems arises from the small energy differences between metal and sulfur valence molecular orbitals, which uniquely poise these systems for dramatic geometric and electronic structure changes as the oxidation state changes. Herein, we have used a combination of resonance Raman, magnetic circular dichroism, electron paramagnetic resonance, and UV photoelectron spectroscopies to explore the electronic states involved in the vibronic coupling mechanism. Comparison between the UV photoelectron spectroscopy (UPS) of the d² M = Mo complex and the resonance Raman spectra of the d¹ M = V complex reveals the power of this combined spectroscopic approach. Here, we observe that the UPS spectrum of Cp₂Mo(bdt) contains an intriguing vibronic progession that is dominated by a "missing-mode" that is composed of PJT-active distortions. We discuss the relationship of the PJT distortions to facile electron transfer in molybdenum enzymes.

Figure 1:

Accepted structures for the active sites of the three canonical Mo enzyme families (top) and the reduced form of the pyranopterin dithiolene cofactor (bottom). R = H or dinucleotide. SO: sulfite oxidase family; XDH: xanthine dehydrogenase family; DMSOR: dimethyl sulfoxide reductase family.

Figure 2:

Frontier molecular orbital diagram for Cp₂M(bdt), (M=Mo,V,Ti). Arrows indicate band assignments of dominant absorption features as discussed in text. S_π⁺ and S_π⁻ refer to the in-phase and out-of-phase sulfur p orbital combinations^, respectively. Orbital notation follows that given previously in the literature, where we have defined the axes such that the metal orbital can be described as dz₂¹. The molybdenum-dithiolene fold is along the S-S vector (red dashed line), resulting in a C_s point group (with the mirror plane in the xy plane). The pseudo Jahn-Teller (PJT) effect is important in the V and Ti compounds. Red line: ligand-based orbital; Blue line: metal-based orbital; Purple line: strongly mixed metal + ligand orbitals.

Figure 3:

Left: Calculated frontier molecular orbitals of 1. Arrow denotes calculated low energy LMCT probed by electronic absorption and rR spectroscopies. Right: The electron density difference map (EDDM) for this LMCT transition (blue: electron loss in the transition, red: electron gain in the transition). The computed composition of the EDDM is ~90% S_π⁺ → d_xy LMCT in character. Isovalues: 0.04 (orbitals), 0.004 (EDDM).

Figure 4A:

Solution (CH₂Cl₂) absorption spectrum and resonance Raman profiles of Cp₂Mo(bdt) (1). Gaussian resolved bands are denoted with Roman numerals. 4B: Experimental (CH₂Cl₂) and theoretical (PBE0) resonance Raman spectra for 1. Experimental excitation wavelength: 488 nm (in resonance with band I), theoretical: 444 nm (in resonance with calculated λ_max). Numbers in the figure denote the vibrational frequencies (normal font: experimental; italic: theoretical).

Figure 5:

A schematic representation of the ionization process. A single ionization band will be constituted by peaks from individual vibrational levels of the cation (left). The reorganization energy, λ_v, here, is taken as the difference in energy between the vertical ionization energy (dotted line) and the adiabatic ionization energy.

Figure 6:

Close-up of the first ionization band of the gas-phase UPS spectrum of Cp₂Mo(bdt) (1). Also shown is the fit for vibrational structure with a Poisson distribution. The spacing of the peaks in the Poisson distribution corresponds to the 383 cm⁻¹ vibronic progression that is activated by ionization from the HOMO of 1.

Figure 7:

Top: Frontier quasi-restricted MOs (QROs) for 2. Right: Arrows denote major transitions in the low-energy visible region. EDDMs for the transitions are given on the right (blue: electron loss, red: electron gain). Isovalues: 0.04 (orbitals), 0.004 (EDDM). Bottom: RT EPR spectrum of 2 (g_iso = 1.9923; A_iso (⁵¹V) = 166 MHz). Note that the Mo(z²) – Sπ+ mixing provides a covalency and charge transfer mechanism for g_iso ~2. Orbital symmetry labels are for the parent (1, C_2v) and distorted (C_s, italic) geometries.

Figure 8.

A: Gaussian deconvoluted solution absorption spectrum (RT) and MCD spectra (5K, 7T) of 2 (M=V). Solvent: 2-Me-THF. Gaussian resolved bands are denoted with roman numerals. Dashed lines are a guide to the eye to show the concurrence between transitions in the MCD and UV-Visible-NIR spectra. B: Experimental (solid, NaCl matrix, Na2SO4 internal standard) and theoretical (PBE0) resonance Raman spectra for 2. Experimental excitation wavelength: 780 nm, theoretical: 855 nm (in resonance with calculated λ_max of band II).

Figure 9:

Depiction of upper (black) and lower (red) potential energy surfaces associated with varying values of F² (Eqn. 5). Dotted: F² = 0, solid: F² = Δ·K₀, dashed: F² = 2Δ·K₀. Note that when the critical condition F² > Δ·K₀ is met, the single-well ground state potential energy surface inverts into a double-well potential. This is the signature description of a strong PJT effect.

Figure 10.

A: Electronic absorption spectrum (CH₂Cl₂) and rR excitation profiles (NaCl/Na₂SO₄) of 3 (M=Ti). Gaussian resolved bands are denoted with roman numerals. B: Experimental (NaCl/Na₂SO₄) and theoretical (PBE0) resonance Raman spectra for 3. Experimental excitation wavelength: 647 nm, theoretical: 500 nm (in resonance with calculated λ_max).

Figure 11:

Frontier molecular orbitals for 3. Arrows denote major transitions in the low-energy LMCT region. EDDMs for the transitions are given on the right (blue: electron loss, red: electron gain). Isovalues: 0.04 (orbitals), 0.004 (EDDM). Orbital symmetry labels are for the parent (1, C_2v) and distorted (C_s, italic) geometries.

Figure 12:

PJT mixing in Cp₂Ti(bdt) of the B₁ excited state with the A₁ ground state results in a distortion and subsequent mixing of the metal and ligand orbitals. Isovalue: 0.04.