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

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.

doi:10.1021/jacs.3c04048

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

Journal Article · Thu Jul 13 00:00:00 EDT 2023 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.3c04048· OSTI ID:1996542

^[1];

^[1]; Kroll, Thomas ^[2]; Sokaras, Dimosthenis ^[2]; Kelemen, Bradley ^[3]; Hedman, Britt ^[2]; Hodgson, Keith O. ^[4];

^[4]

Stanford Univ., CA (United States)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
IFF Health and Biosciences, Palo Alto, CA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

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. Here, 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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; P30GM133894

OSTI ID:: 1996542

Journal Information:: Journal of the American Chemical Society, Vol. 145, Issue 29; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
crystal cleavage
electronic structure
energy
ligands
molecular structure

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

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