Electron transfer in polysaccharide monooxygenase catalysis

Sayler, Richard I.; Thomas, William C.; Rose, Alexander J.; Marletta, Michael A.

doi:10.1073/pnas.2411229121

Electron transfer in polysaccharide monooxygenase catalysis

Journal Article · Mon Dec 30 00:00:00 EST 2024 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2411229121· OSTI ID:2484077

; Thomas, William C.; Rose, Alexander J.;

Polysaccharide monooxygenase (PMO) catalysis involves the chemically difficult hydroxylation of unactivated C–H bonds in carbohydrates. The reaction requires reducing equivalents and will utilize either oxygen or hydrogen peroxide as a cosubstrate. Two key mechanistic questions are addressed here: 1) How does the enzyme regulate the timely and tightly controlled electron delivery to the mononuclear copper active site, especially when bound substrate occludes the active site? and 2) How does this electron delivery differ when utilizing oxygen or hydrogen peroxide as a cosubstrate? Using a computational approach, potential paths of electron transfer (ET) to the active site copper ion were identified in a representative AA9 family PMO from Myceliophthora thermophila ( Mt PMO9E). When Y62, a buried residue 12 Å from the active site, is mutated to F, lower activity is observed with O ₂ . However, a WT-level activity is observed with H ₂ O ₂ as a cosubstrate indicating an important role in ET for O ₂ activation. To better understand the structural effects of mutations to Y62 and axial copper ligand Y168, crystal structures were solved of the wild type Mt PMO9E and the variants Y62W, Y62F, and Y168F. A bioinformatic analysis revealed that position 62 is conserved as either Y or W in the AA9 family. The Mt PMO9E Y62W variant has restored activity with O ₂ . Overall, the use of redox-active residues to supply electrons for the reaction with O ₂ appears to be widespread in the AA9 family. Furthermore, the results provide a molecular framework to understand catalysis with O ₂ versus H ₂ O ₂ .

View Journal Article

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2484077

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 1 Vol. 122; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (48)

Electron Transfer in Peptides with Cysteine and Methionine as Relay Amino Acids Wang, Min; Gao, Jian; Müller, Pavel Angewandte Chemie International Edition, Vol. 48, Issue 23 https://doi.org/10.1002/anie.200900827	journal	May 2009
Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase O'Dell, William B.; Agarwal, Pratul K.; Meilleur, Flora Angewandte Chemie International Edition, Vol. 56, Issue 3 https://doi.org/10.1002/anie.201610502	journal	December 2016
A tale of two methane monooxygenases Ross, Matthew O.; Rosenzweig, Amy C. JBIC Journal of Biological Inorganic Chemistry, Vol. 22, Issue 2-3 https://doi.org/10.1007/s00775-016-1419-y	journal	November 2016
Structural perturbations of substrate binding and oxidation state changes in a lytic polysaccharide monooxygenase Walton, Paul H.; Davies, Gideon J. JBIC Journal of Biological Inorganic Chemistry, Vol. 27, Issue 8 https://doi.org/10.1007/s00775-022-01966-z	journal	October 2022
The one-electron transfer redox potentials of free radicals. I. The oxygen/superoxide system Ilan, Yael A.; Czapski, Gidon; Meisel, Dan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 430, Issue 2 https://doi.org/10.1016/0005-2728(76)90080-3	journal	May 1976
Oxidation: An important enzyme reaction in fungal degradation of cellulose Eriksson, Karl-Erik; Pettersson, Bert; Westermark, Ulla FEBS Letters, Vol. 49, Issue 2 https://doi.org/10.1016/0014-5793(74)80531-4	journal	December 1974
Electrode potentials of partially reduced oxygen species, from dioxygen to water Koppenol, Willem H.; Stanbury, David M.; Bounds, Patricia L. Free Radical Biology and Medicine, Vol. 49, Issue 3 https://doi.org/10.1016/j.freeradbiomed.2010.04.011	journal	August 2010
EFI-EST, EFI-GNT, and EFI-CGFP: Enzyme Function Initiative (EFI) Web Resource for Genomic Enzymology Tools Oberg, Nils; Zallot, Rémi; Gerlt, John A. Journal of Molecular Biology, Vol. 435, Issue 14 https://doi.org/10.1016/j.jmb.2023.168018	journal	July 2023
Recent insights into copper-containing lytic polysaccharide mono-oxygenases Hemsworth, Glyn R.; Davies, Gideon J.; Walton, Paul H. Current Opinion in Structural Biology, Vol. 23, Issue 5, p. 660-668 https://doi.org/10.1016/j.sbi.2013.05.006	journal	October 2013
Polysaccharide degradation by lytic polysaccharide monooxygenases Forsberg, Zarah; Sørlie, Morten; Petrović, Dejan Current Opinion in Structural Biology, Vol. 59 https://doi.org/10.1016/j.sbi.2019.02.015	journal	December 2019
Structural Basis for Substrate Targeting and Catalysis by Fungal Polysaccharide Monooxygenases Li, Xin; Beeson, William T.; Phillips, Christopher M. Structure, Vol. 20, Issue 6, p. 1051-1061 https://doi.org/10.1016/j.str.2012.04.002	journal	June 2012
Lytic Polysaccharide Monooxygenases in Biomass Conversion Hemsworth, Glyn R.; Johnston, Esther M.; Davies, Gideon J. Trends in Biotechnology, Vol. 33, Issue 12 https://doi.org/10.1016/j.tibtech.2015.09.006	journal	December 2015
Glycosidic Bond Hydroxylation by Polysaccharide Monooxygenases Hangasky, John A.; Detomasi, Tyler C.; Marletta, Michael A. Trends in Chemistry, Vol. 1, Issue 2 https://doi.org/10.1016/j.trechm.2019.01.007	journal	May 2019
A Random-Sequential Kinetic Mechanism for Polysaccharide Monooxygenases Hangasky, John A.; Marletta, Michael A. Biochemistry, Vol. 57, Issue 22 https://doi.org/10.1021/acs.biochem.8b00129	journal	April 2018
Catalytic Mechanism of Fungal Lytic Polysaccharide Monooxygenases Investigated by First-Principles Calculations Bertini, Luca; Breglia, Raffaella; Lambrughi, Matteo Inorganic Chemistry, Vol. 57, Issue 1 https://doi.org/10.1021/acs.inorgchem.7b02005	journal	December 2017
Two Aromatic Rings Coupled a Sulfur-Containing Group to Favor Protein Electron Transfer by Instantaneous Formations of π∴S:π↔π:S∴π or π∴π:S↔π:π∴S Five-Electron Bindings Sun, Weichao; Ren, Haisheng; Tao, Ye The Journal of Physical Chemistry C, Vol. 119, Issue 17 https://doi.org/10.1021/acs.jpcc.5b01740	journal	April 2015
The Role of the Secondary Coordination Sphere in a Fungal Polysaccharide Monooxygenase Span, Elise A.; Suess, Daniel L. M.; Deller, Marc C. ACS Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1021/acschembio.7b00016	journal	March 2017
Cellobiose Dehydrogenase and a Copper-Dependent Polysaccharide Monooxygenase Potentiate Cellulose Degradation by Neurospora crassa Phillips, Christopher M.; Beeson, William T.; Cate, Jamie H. ACS Chemical Biology, Vol. 6, Issue 12, p. 1399-1406 https://doi.org/10.1021/cb200351y	journal	December 2011
Mechanisms Whereby Mononuclear Copper Proteins Functionalize Organic Substrates Klinman, Judith P. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950047g	journal	January 1996
Formation of a Copper(II)–Tyrosyl Complex at the Active Site of Lytic Polysaccharide Monooxygenases Following Oxidation by H₂O₂ Paradisi, Alessandro; Johnston, Esther M.; Tovborg, Morten Journal of the American Chemical Society, Vol. 141, Issue 46 https://doi.org/10.1021/jacs.9b09833	journal	November 2019
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2 Bissaro, Bastien; Røhr, Åsmund K.; Müller, Gerdt Nature Chemical Biology, Vol. 13, Issue 10 https://doi.org/10.1038/nchembio.2470	journal	August 2017
Mutational dissection of a hole hopping route in a lytic polysaccharide monooxygenase (LPMO) Ayuso-Fernández, Iván; Emrich-Mills, Tom Z.; Haak, Julia Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-48245-w	journal	May 2024
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
AlphaFill: enriching AlphaFold models with ligands and cofactors Hekkelman, Maarten L.; de Vries, Ida; Joosten, Robbie P. Nature Methods, Vol. 20, Issue 2 https://doi.org/10.1038/s41592-022-01685-y	journal	November 2022
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
The role of the active site tyrosine in the mechanism of lytic polysaccharide monooxygenase McEvoy, Aina; Creutzberg, Joel; Singh, Raushan K. Chemical Science, Vol. 12, Issue 1 https://doi.org/10.1039/D0SC05262K	journal	January 2021
On the roles of methionine and the importance of its microenvironments in redox metalloproteins Gibbs, Curtis A.; Fedoretz-Maxwell, Brooklyn P.; Warren, Jeffrey J. Dalton Transactions, Vol. 51, Issue 13 https://doi.org/10.1039/D1DT04387K	journal	January 2022
Functional and protective hole hopping in metalloenzymes Gray, Harry B.; Winkler, Jay R. Chemical Science, Vol. 12, Issue 42 https://doi.org/10.1039/D1SC04286F	journal	January 2021
Capture of activated dioxygen intermediates at the copper-active site of a lytic polysaccharide monooxygenase Schröder, Gabriela C.; O'Dell, William B.; Webb, Simon P. Chemical Science, Vol. 13, Issue 45 https://doi.org/10.1039/D2SC05031E	journal	January 2022
Revisiting the role of electron donors in lytic polysaccharide monooxygenase biochemistry Hemsworth, Glyn R. Essays in Biochemistry, Vol. 67, Issue 3 https://doi.org/10.1042/EBC20220164	journal	April 2023
Long-range electron transfer Gray, H. B.; Winkler, J. R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 10 https://doi.org/10.1073/pnas.0408029102	journal	February 2005
Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components Quinlan, R. J.; Sweeney, M. D.; Lo Leggio, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 37, p. 15079-15084 https://doi.org/10.1073/pnas.1105776108	journal	August 2011
Interactions of a fungal lytic polysaccharide monooxygenase with β-glucan substrates and cellobiose dehydrogenase Courtade, Gaston; Wimmer, Reinhard; Røhr, Åsmund K. Proceedings of the National Academy of Sciences, Vol. 113, Issue 21 https://doi.org/10.1073/pnas.1602566113	journal	May 2016
Reactivity of O 2 versus H 2 O 2 with polysaccharide monooxygenases Hangasky, John A.; Iavarone, Anthony T.; Marletta, Michael A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 19 https://doi.org/10.1073/pnas.1801153115	journal	April 2018
Mapping hole hopping escape routes in proteins Teo, Ruijie D.; Wang, Ruobing; Smithwick, Elizabeth R. Proceedings of the National Academy of Sciences, Vol. 116, Issue 32 https://doi.org/10.1073/pnas.1906394116	journal	July 2019
Kinetic analysis of amino acid radicals formed in H ₂ O ₂ -driven Cu ^I LPMO reoxidation implicates dominant homolytic reactivity Jones, Stephen M.; Transue, Wesley J.; Meier, Katlyn K. Proceedings of the National Academy of Sciences, Vol. 117, Issue 22 https://doi.org/10.1073/pnas.1922499117	journal	May 2020
Characterization of a unique polysaccharide monooxygenase from the plant pathogen Magnaporthe oryzae Martinez-D’Alto, Alejandra; Yan, Xia; Detomasi, Tyler C. Proceedings of the National Academy of Sciences, Vol. 120, Issue 8 https://doi.org/10.1073/pnas.2215426120	journal	February 2023
Kinetics of H 2 O 2 -driven degradation of chitin by a bacterial lytic polysaccharide monooxygenase Kuusk, Silja; Bissaro, Bastien; Kuusk, Piret Journal of Biological Chemistry, Vol. 293, Issue 2 https://doi.org/10.1074/jbc.M117.817593	journal	November 2017
The Copper-Enzyme Family of Dopamine β-Monooxygenase and Peptidylglycine α-Hydroxylating Monooxygenase: Resolving the Chemical Pathway for Substrate Hydroxylation Klinman, Judith P. Journal of Biological Chemistry, Vol. 281, Issue 6 https://doi.org/10.1074/jbc.R500011200	journal	November 2005
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
Changes in active-site geometry on X-ray photoreduction of a lytic polysaccharide monooxygenase active-site copper and saccharide binding Tandrup, Tobias; Muderspach, Sebastian J.; Banerjee, Sanchari IUCrJ, Vol. 9, Issue 5 https://doi.org/10.1107/S2052252522007175	journal	August 2022
Insights into the H ₂ O ₂ ‐driven catalytic mechanism of fungal lytic polysaccharide monooxygenases Hedison, Tobias M.; Breslmayr, Erik; Shanmugam, Muralidharan The FEBS Journal, Vol. 288, Issue 13 https://doi.org/10.1111/febs.15704	journal	January 2021
On the expansion of biological functions of lytic polysaccharide monooxygenases Vandhana, Theruvothu Madathil; Reyre, Jean‐Lou; Sushmaa, Dangudubiyyam New Phytologist, Vol. 233, Issue 6 https://doi.org/10.1111/nph.17921	journal	January 2022
The crystal structure of human dopamine β-hydroxylase at 2.9 Å resolution Vendelboe, Trine V.; Harris, Pernille; Zhao, Yuguang Science Advances, Vol. 2, Issue 4 https://doi.org/10.1126/sciadv.1500980	journal	April 2016
Recovery of particulate methane monooxygenase structure and activity in a lipid bilayer Koo, Christopher W.; Tucci, Frank J.; He, Yuan Science, Vol. 375, Issue 6586 https://doi.org/10.1126/science.abm3282	journal	March 2022
A moonlighting function of a chitin polysaccharide monooxygenase, CWR-1, in Neurospora crassa allorecognition Detomasi, Tyler C.; Rico-Ramírez, Adriana M.; Sayler, Richard I. eLife, Vol. 11 https://doi.org/10.7554/eLife.80459	journal	August 2022

Similar Records

Insights into an unusual Auxiliary Activity 9 family member lacking the histidine brace motif of lytic polysaccharide monooxygenases

Journal Article · Thu Aug 29 20:00:00 EDT 2019 · Journal of Biological Chemistry · OSTI ID:1619137

Role for Threonine 201 in the Catalytic Cycle of the Soluble Diiron Hydroxylase Toluene 4-Monooxygenase

Journal Article · Mon Jun 01 00:00:00 EDT 2009 · Biochemistry-US · OSTI ID:1005632

Electron transfer in polysaccharide monooxygenase catalysis

Citation Formats

References (48)

Similar Records

Related Subjects