Kβ X‑ray Emission Spectroscopy of Cu(I)-Lytic Polysaccharide Monooxygenase: Direct Observation of the Frontier Molecular Orbital for H2O2 Activation

• Published in: Journal of the American Chemical Society Vol. 145; no. 29; pp. 16015 - 16025
• Main Authors: Lim, Hyeongtaek, Brueggemeyer, Magdalene T., Transue, Wesley J., Meier, Katlyn K., Jones, Stephen M., Kroll, Thomas, Sokaras, Dimosthenis, Kelemen, Bradley, Hedman, Britt, Hodgson, Keith O., Solomon, Edward I.
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 26.07.2023; American Chemical Society (ACS)
• Subjects: active sites; crystal cleavage; density functional theory; electronic structure; energy; geometry; histidine; homolytic cleavage; INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; ligands; molecular structure; polysaccharides; spectroscopy; X-radiation
• ISSN: 0002-7863; 1520-5126; 1520-5126
• DOI: 10.1021/jacs.3c04048

Lytic polysaccharide monooxygenases (LPMOs) catalyze the degradation of recalcitrant carbohydrate polysaccharide substrates. These enzymes are characterized by a mononuclear Cu­(I) active site with a three-coordinate T-shaped “His-brace” configuration including the N-terminal histidine and its amine group as ligands. This study explicitly investigates the electronic structure of the d10 Cu­(I) active site in a LPMO using Kβ X-ray emission spectroscopy (XES). The lack of inversion symmetry in the His-brace site enables the 3d/p mixing required for intensity in the Kβ valence-to-core (VtC) XES spectrum of Cu­(I)-LPMO. These Kβ XES data are correlated to density functional theory (DFT) calculations to define the bonding, and in particular, the frontier molecular orbital (FMO) of the Cu­(I) site. These experimentally validated DFT calculations are used to evaluate the reaction coordinate for homolytic cleavage of the H2O2 O–O bond and understand the contribution of this FMO to the low barrier of this reaction and how the geometric and electronic structure of the Cu­(I)-LPMO site is activated for rapid reactivity with H2O2.