Nitrous oxide (N2O) contributes significantly to ozone layer depletion and is a potent greenhouse agent, motivating interest in the chemical details of biological N2O fixation by nitrous oxide reductase (N2OR) during bacterial denitrification. In this study, we report a combined experimental/computational study of a synthetic [4Cu:1S] cluster supported by N-donor ligands that can be considered the closest structural and functional mimic of the CuZ catalytic site in N2OR reported to date. Quantitative N2 measurements during synthetic N2O reduction were used to determine reaction stoichiometry, which in turn was used as the basis for density functional theory (DFT) modeling of hypothetical reaction intermediates. The mechanism for N2O reduction emerging from this computational modeling involves cooperative activation of N2O across a Cu/S cluster edge. Direct interaction of the μ4-S ligand with the N2O substrate during coordination and N-O bond cleavage represents an unconventional mechanistic paradigm to be considered for the chemistry of CuZ and related metal-sulfur clusters. Consistent with hypothetical participation of the μ4-S unit in two-electron reduction of N2O, Cu K-edge and S K-edge X-ray absorption spectroscopy (XAS) reveal a high degree of participation by the μ4-S in redox changes, with approximately 21% S 3p contribution to the redox-active molecular orbital in the highly covalent [4Cu:1S] core, compared to approximately 14% Cu 3d contribution per copper. The XAS data included in this study represent the first spectroscopic interrogation of multiple redox levels of a [4Cu:1S] cluster and show high fidelity to the biological CuZ site.
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