Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase

O'Dell, William B.; Agarwal, Pratul K.; Meilleur, Flora

doi:10.1002/ange.201610502

Title: Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase

Journal Article · Thu Dec 22 00:00:00 EST 2016 · Angewandte Chemie

DOI:https://doi.org/10.1002/ange.201610502· OSTI ID:1407721

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Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Dept. of Molecular and Structural Biochemistry
Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemisty, Cellular and Molecular Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Knoxville and Computatinal Biology Inst., Computer Science, Mathematics Division

Lytic polysaccharide monooxygenases have attracted vast attention owing to their abilities to disrupt glycosidic bonds via oxidation instead of hydrolysis and to enhance enzymatic digestion of recalcitrant substrates including chitin and cellulose. Here, we determined the high-resolution X-ray crystal structures of an enzyme from Neurospora crassa in the resting state and of a copper(II) dioxo intermediate complex formed in the absence of substrate. X-ray crystal structures also revealed “pre-bound” molecular oxygen adjacent to the active site. An examination of protonation states enabled by neutron crystallography and density functional theory calculations identified a role for a conserved histidine in promoting oxygen activation. Our results provide a new structural description of oxygen activation by substrate free lytic polysaccharide monooxygenases and provide insights that can be extended to reactivity in the enzyme–substrate complex.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC05-00OR22725; MRI 09229719; IGERT 1069091; GM105978

OSTI ID:: 1407721

Journal Information:: Angewandte Chemie, Vol. 129, Issue 3; ISSN 0044-8249

Publisher:: German Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Detection and Characterization of a Novel Copper‐Dependent Intermediate in a Lytic Polysaccharide Monooxygenase Singh, Raushan K.; Blossom, Benedikt M.; Russo, David A. Chemistry – A European Journal, Vol. 26, Issue 2 https://doi.org/10.1002/chem.201903562	journal	November 2019
Molecular mechanism of lytic polysaccharide monooxygenases Hedegård, Erik Donovan; Ryde, Ulf Chemical Science, Vol. 9, Issue 15 https://doi.org/10.1039/c8sc00426a	journal	January 2018
Is density functional theory accurate for lytic polysaccharide monooxygenase enzymes? Larsson, Ernst D.; Dong, Geng; Veryazov, Valera Dalton Transactions, Vol. 49, Issue 5 https://doi.org/10.1039/c9dt04486h	journal	January 2020
Iron oxides with a reverse spinel structure: impact of active sites on molecule adsorption Jian, Wei; Jia, Ran; Wang, Jian Inorganic Chemistry Frontiers, Vol. 6, Issue 10 https://doi.org/10.1039/c9qi00790c	journal	January 2019
Molecular mechanism of the chitinolytic peroxygenase reaction Bissaro, Bastien; Streit, Bennett; Isaksen, Ingvild Proceedings of the National Academy of Sciences, Vol. 117, Issue 3 https://doi.org/10.1073/pnas.1904889117	journal	January 2020
Molecular mechanism of the chitinolytic monocopper peroxygenase reaction Bissaro, Bastien; Streit, Bennett; Isaksen, Ingvild Proceedings of the National Academy of Sciences https://doi.org/10.1101/541292	journal	February 2019
Structural and molecular dynamics studies of a C1‐oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition Liu, Bing; Kognole, Abhishek A.; Wu, Miao The FEBS Journal, Vol. 285, Issue 12 https://doi.org/10.1111/febs.14472	journal	April 2018
Polysaccharide oxidation by lytic polysaccharide monooxygenase is enhanced by engineered cellobiose dehydrogenase Kracher, Daniel; Forsberg, Zarah; Bissaro, Bastien The FEBS Journal, Vol. 287, Issue 5 https://doi.org/10.1111/febs.15067	journal	October 2019
Biochemical studies of two lytic polysaccharide monooxygenases from the white-rot fungus Heterobasidion irregulare and their roles in lignocellulose degradation Liu, Bing; Olson, Åke; Wu, Miao PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0189479	journal	December 2017
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Targeting the reactive intermediate in polysaccharide monooxygenases Hedegård, Erik D.; Ryde, Ulf JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 7 https://doi.org/10.1007/s00775-017-1480-1	journal	July 2017

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
copper
oxidoreductases
oxygen activation
polysaccharide monooxygenases
protein structures

Title: Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase

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