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Title: Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation

Abstract

A new paradigm for cellulose depolymerization by fungi focuses on an oxidative mechanism involving cellobiose dehydrogenases (CDH) and copper-dependent lytic polysaccharide monooxygenases (LPMO); however, mechanistic studies have been hampered by the lack of structural information regarding CDH. CDH contains a haem-binding cytochrome (CYT) connected via a flexible linker to a flavin-dependent dehydrogenase (DH). Electrons are generated from cellobiose oxidation catalysed by DH and shuttled via CYT to LPMO. Here we present structural analyses that provide a comprehensive picture of CDH conformers, which govern the electron transfer between redox centres. Using structure-based site-directed mutagenesis, rapid kinetics analysis and molecular docking, we demonstrate that flavin-to-haem interdomain electron transfer (IET) is enabled by a haem propionate group and that rapid IET requires a closed CDH state in which the propionate is tightly enfolded by DH. Following haem reduction, CYT reduces LPMO to initiate oxygen activation at the copper centre and subsequent cellulose depolymerization.

Authors:
 [1];  [2];  [1];  [2];  [2];  [2];  [3];  [2];  [1]
+ Show Author Affiliations
  1. KTH Royal Inst. of Technology, Stockholm (Sweden). School of Biotechnology; Karolinska Inst., Stockholm (Sweden). Dept. of Medical Biochemistry
  2. Univ. of Natural Resources and Life Sciences, Vienna (Austria). Food Biotechnology Lab. Dept. of Food Science and Technology
  3. Karolinska Inst., Stockholm (Sweden). Dept. of Cell and Molecular Biology; European Molecular Biology Lab. (EMBL), Hamburg (Germany); Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany). Centre for Structural Systems Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1623985
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Tan, Tien-Chye, Kracher, Daniel, Gandini, Rosaria, Sygmund, Christoph, Kittl, Roman, Haltrich, Dietmar, Hällberg, B. Martin, Ludwig, Roland, and Divne, Christina. Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. United States: N. p., 2015. Web. doi:10.1038/ncomms8542.
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Tan, Tien-Chye, Kracher, Daniel, Gandini, Rosaria, Sygmund, Christoph, Kittl, Roman, Haltrich, Dietmar, Hällberg, B. Martin, Ludwig, Roland, & Divne, Christina. Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. United States. https://doi.org/10.1038/ncomms8542
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Tan, Tien-Chye, Kracher, Daniel, Gandini, Rosaria, Sygmund, Christoph, Kittl, Roman, Haltrich, Dietmar, Hällberg, B. Martin, Ludwig, Roland, and Divne, Christina. Tue . "Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation". United States. https://doi.org/10.1038/ncomms8542. https://www.osti.gov/servlets/purl/1623985.
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@article{osti_1623985,
title = {Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation},
author = {Tan, Tien-Chye and Kracher, Daniel and Gandini, Rosaria and Sygmund, Christoph and Kittl, Roman and Haltrich, Dietmar and Hällberg, B. Martin and Ludwig, Roland and Divne, Christina},
abstractNote = {A new paradigm for cellulose depolymerization by fungi focuses on an oxidative mechanism involving cellobiose dehydrogenases (CDH) and copper-dependent lytic polysaccharide monooxygenases (LPMO); however, mechanistic studies have been hampered by the lack of structural information regarding CDH. CDH contains a haem-binding cytochrome (CYT) connected via a flexible linker to a flavin-dependent dehydrogenase (DH). Electrons are generated from cellobiose oxidation catalysed by DH and shuttled via CYT to LPMO. Here we present structural analyses that provide a comprehensive picture of CDH conformers, which govern the electron transfer between redox centres. Using structure-based site-directed mutagenesis, rapid kinetics analysis and molecular docking, we demonstrate that flavin-to-haem interdomain electron transfer (IET) is enabled by a haem propionate group and that rapid IET requires a closed CDH state in which the propionate is tightly enfolded by DH. Following haem reduction, CYT reduces LPMO to initiate oxygen activation at the copper centre and subsequent cellulose depolymerization.},
doi = {10.1038/ncomms8542},
journal = {Nature Communications},
number = 1,
volume = 6,
place = {United States},
year = {Tue Jul 07 00:00:00 EDT 2015},
month = {Tue Jul 07 00:00:00 EDT 2015}
}
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    Multiplicity of enzymatic functions in the CAZy AA3 family
    journal, February 2018

    • Sützl, Leander; Laurent, Christophe V. F. P.; Abrera, Annabelle T.
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 6
    • DOI: 10.1007/s00253-018-8784-0

    Biocatalytic Oxidation Reactions: A Chemist's Perspective
    journal, July 2018

    • Dong, JiaJia; Fernández-Fueyo, Elena; Hollmann, Frank
    • Angewandte Chemie International Edition, Vol. 57, Issue 30
    • DOI: 10.1002/anie.201800343

    Discovery, activity and characterisation of an AA10 lytic polysaccharide oxygenase from the shipworm symbiont Teredinibacter turnerae
    journal, September 2019

    • Fowler, Claire. A.; Sabbadin, Federico; Ciano, Luisa
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1573-x

    Direct Electron Transfer of Dehydrogenases for Development of 3rd Generation Biosensors and Enzymatic Fuel Cells
    journal, April 2018

    • Bollella, Paolo; Gorton, Lo; Antiochia, Riccarda
    • Sensors, Vol. 18, Issue 5
    • DOI: 10.3390/s18051319

    Molecular and catalytic properties of fungal extracellular cellobiose dehydrogenase produced in prokaryotic and eukaryotic expression systems
    journal, February 2017

    Isolation of homogeneous polysaccharide monooxygenases from fungal sources and investigation of their synergism with cellulases when acting on cellulose
    journal, May 2016

    Plant–necrotroph co-transcriptome networks illuminate a metabolic battlefield
    journal, May 2019

    • Zhang, Wei; Corwin, Jason A.; Copeland, Daniel Harrison
    • eLife, Vol. 8
    • DOI: 10.7554/elife.44279

    Molecular mechanism of lytic polysaccharide monooxygenases
    text, January 2018

    Polysaccharide monooxygenase-catalyzed oxidation of cellulose to glucuronic acid-containing cello-oligosaccharides
    journal, February 2019

    Direct Electron Transfer of Dehydrogenases for Development of 3rd Generation Biosensors and Enzymatic Fuel Cells
    journal, April 2018

    • Bollella, Paolo; Gorton, Lo; Antiochia, Riccarda
    • Sensors, Vol. 18, Issue 5
    • DOI: 10.3390/s18051319

    Polysaccharide oxidation by lytic polysaccharide monooxygenase is enhanced by engineered cellobiose dehydrogenase
    journal, October 2019

    • Kracher, Daniel; Forsberg, Zarah; Bissaro, Bastien
    • The FEBS Journal, Vol. 287, Issue 5
    • DOI: 10.1111/febs.15067

    Molecular and catalytic properties of fungal extracellular cellobiose dehydrogenase produced in prokaryotic and eukaryotic expression systems
    journal, February 2017

    Insights into the mechanism(s) of digestion of crystalline cellulose by plant class C GH9 endoglucanases
    journal, July 2019

    On the functional characterization of lytic polysaccharide monooxygenases (LPMOs)
    journal, March 2019

    • Eijsink, Vincent G. H.; Petrovic, Dejan; Forsberg, Zarah
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1392-0

    Myceliophthora thermophila M77 utilizes hydrolytic and oxidative mechanisms to deconstruct biomass
    journal, November 2016

    • dos Santos, Hévila Brognaro; Bezerra, Thaís Milena Souza; Pradella, José G. C.
    • AMB Express, Vol. 6, Issue 1
    • DOI: 10.1186/s13568-016-0276-y

    Direct Electron Transfer of Enzymes Facilitated by Cytochromes
    journal, January 2019

    Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme
    journal, April 2016

    • Cannella, D.; Möllers, K. B.; Frigaard, N. -U.
    • Nature Communications, Vol. 7, Issue 1
    • DOI: 10.1038/ncomms11134

    A fungal family of lytic polysaccharide monooxygenase-like copper proteins
    journal, January 2020

    • Labourel, Aurore; Frandsen, Kristian E. H.; Zhang, Feng
    • Nature Chemical Biology, Vol. 16, Issue 3
    • DOI: 10.1038/s41589-019-0438-8

    Polysaccharide monooxygenase-catalyzed oxidation of cellulose to glucuronic acid-containing cello-oligosaccharides
    journal, February 2019

    Sequence and Structural Analysis of AA9 and AA10 LPMOs: An Insight into the Basis of Substrate Specificity and Regioselectivity
    journal, September 2019

    • Zhou, Xiaoli; Qi, Xiaohua; Huang, Hongxia
    • International Journal of Molecular Sciences, Vol. 20, Issue 18
    • DOI: 10.3390/ijms20184594

    Reactivity of O 2 versus H 2 O 2 with polysaccharide monooxygenases
    journal, April 2018

    • Hangasky, John A.; Iavarone, Anthony T.; Marletta, Michael A.
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 19
    • DOI: 10.1073/pnas.1801153115

    Myceliophthora thermophila M77 utilizes hydrolytic and oxidative mechanisms to deconstruct biomass
    journal, November 2016

    • dos Santos, Hévila Brognaro; Bezerra, Thaís Milena Souza; Pradella, José G. C.
    • AMB Express, Vol. 6, Issue 1
    • DOI: 10.1186/s13568-016-0276-y

    On the functional characterization of lytic polysaccharide monooxygenases (LPMOs)
    journal, March 2019

    • Eijsink, Vincent G. H.; Petrovic, Dejan; Forsberg, Zarah
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1392-0

    Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme
    journal, April 2016

    • Cannella, D.; Möllers, K. B.; Frigaard, N. -U.
    • Nature Communications, Vol. 7, Issue 1
    • DOI: 10.1038/ncomms11134

    Multiplicity of enzymatic functions in the CAZy AA3 family
    journal, February 2018

    • Sützl, Leander; Laurent, Christophe V. F. P.; Abrera, Annabelle T.
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 6
    • DOI: 10.1007/s00253-018-8784-0

    Heterogeneity in the Histidine-brace Copper Coordination Sphere in Auxiliary Activity Family 10 (AA10) Lytic Polysaccharide Monooxygenases
    journal, April 2016

    • Chaplin, Amanda K.; Wilson, Michael T.; Hough, Michael A.
    • Journal of Biological Chemistry, Vol. 291, Issue 24, p. 12838-12850
    • DOI: 10.1074/jbc.m116.722447

    Biokatalytische Oxidationsreaktionen - aus der Sicht eines Chemikers
    journal, July 2018

    • Dong, JiaJia; Fernández-Fueyo, Elena; Hollmann, Frank
    • Angewandte Chemie, Vol. 130, Issue 30
    • DOI: 10.1002/ange.201800343

    Biocatalytic Oxidation Reactions: A Chemist's Perspective
    journal, July 2018

    • Dong, JiaJia; Fernández-Fueyo, Elena; Hollmann, Frank
    • Angewandte Chemie International Edition, Vol. 57, Issue 30
    • DOI: 10.1002/anie.201800343

    How to break down crystalline cellulose
    journal, May 2016

    Molecular Mechanisms of Oxygen Activation and Hydrogen Peroxide Formation in Lytic Polysaccharide Monooxygenases
    journal, April 2019

    The GMC superfamily of oxidoreductases revisited: analysis and evolution of fungal GMC oxidoreductases
    journal, May 2019

    • Sützl, Leander; Foley, Gabriel; Gillam, Elizabeth M. J.
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1457-0

    Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose
    journal, June 2016

    • Garajova, Sona; Mathieu, Yann; Beccia, Maria Rosa
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep28276

    The H2O2-dependent activity of a fungal lytic polysaccharide monooxygenase investigated with a turbidimetric assay
    journal, March 2020

    Extracellular electron transfer systems fuel cellulose oxidative degradation
    journal, April 2016

    The Pyrroloquinoline-Quinone-Dependent Pyranose Dehydrogenase from Coprinopsis cinerea Drives Lytic Polysaccharide Monooxygenase Action
    journal, June 2018

    • Várnai, Anikó; Umezawa, Kiwamu; Yoshida, Makoto
    • Applied and Environmental Microbiology, Vol. 84, Issue 11
    • DOI: 10.1128/aem.00156-18

    Lytic polysaccharide monooxygenases from Myceliophthora thermophila C1 differ in substrate preference and reducing agent specificity
    journal, August 2016

    • Frommhagen, Matthias; Koetsier, Martijn J.; Westphal, Adrie H.
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0594-y

    Activation of bacterial lytic polysaccharide monooxygenases with cellobiose dehydrogenase: Activation of Bacterial LPMOs with CDH
    journal, September 2016

    • Loose, Jennifer S. M.; Forsberg, Zarah; Kracher, Daniel
    • Protein Science, Vol. 25, Issue 12
    • DOI: 10.1002/pro.3043

    Studying Direct Electron Transfer by Site‐Directed Immobilization of Cellobiose Dehydrogenase
    journal, September 2018

    • Meneghello, Marta; Al‐Lolage, Firas A.; Ma, Su
    • ChemElectroChem, Vol. 6, Issue 3
    • DOI: 10.1002/celc.201801503

    Regioselectivity of oxidation by a polysaccharide monooxygenase from Chaetomium thermophilum
    journal, June 2018

    Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus
    journal, April 2020

    The Pyrroloquinoline-Quinone-Dependent Pyranose Dehydrogenase from Coprinopsis cinerea Drives Lytic Polysaccharide Monooxygenase Action
    journal, June 2018

    • Várnai, Anikó; Umezawa, Kiwamu; Yoshida, Makoto
    • Applied and Environmental Microbiology, Vol. 84, Issue 11
    • DOI: 10.1128/aem.00156-18

    Sequence and Structural Analysis of AA9 and AA10 LPMOs: An Insight into the Basis of Substrate Specificity and Regioselectivity
    journal, September 2019

    • Zhou, Xiaoli; Qi, Xiaohua; Huang, Hongxia
    • International Journal of Molecular Sciences, Vol. 20, Issue 18
    • DOI: 10.3390/ijms20184594

    Learning from microbial strategies for polysaccharide degradation
    journal, February 2016

    • Hemsworth, Glyn R.; Déjean, Guillaume; Davies, Gideon J.
    • Biochemical Society Transactions, Vol. 44, Issue 1
    • DOI: 10.1042/bst20150180

    The H2O2-dependent activity of a fungal lytic polysaccharide monooxygenase investigated with a turbidimetric assay
    journal, March 2020

    Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass
    journal, September 2018

    • Bissaro, Bastien; Várnai, Anikó; Røhr, Åsmund K.
    • Microbiology and Molecular Biology Reviews, Vol. 82, Issue 4
    • DOI: 10.1128/mmbr.00029-18

    Distinct Substrate Specificities and Electron-Donating Systems of Fungal Lytic Polysaccharide Monooxygenases
    journal, May 2018

    • Frommhagen, Matthias; Westphal, Adrie H.; van Berkel, Willem J. H.
    • Frontiers in Microbiology, Vol. 9
    • DOI: 10.3389/fmicb.2018.01080

    Lytic polysaccharide monooxygenases and other oxidative enzymes are abundantly secreted by Aspergillus nidulans grown on different starches
    journal, September 2016

    • Nekiunaite, Laura; Arntzen, Magnus Ø.; Svensson, Birte
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0604-0

    Activity, stability and 3-D structure of the Cu( ii ) form of a chitin-active lytic polysaccharide monooxygenase from Bacillus amyloliquefaciens
    journal, January 2016

    • Gregory, Rebecca C.; Hemsworth, Glyn R.; Turkenburg, Johan P.
    • Dalton Transactions, Vol. 45, Issue 42, p. 16904-16912
    • DOI: 10.1039/c6dt02793h

    Salt-responsive lytic polysaccharide monooxygenases from the mangrove fungus Pestalotiopsis sp. NCi6
    journal, May 2016

    Direct Electron Transfer of Enzymes Facilitated by Cytochromes
    journal, December 2018

    Crystal Structure of the Catalytic and Cytochrome b Domains in a Eukaryotic Pyrroloquinoline Quinone-Dependent Dehydrogenase
    journal, October 2019

    • Takeda, Kouta; Ishida, Takuya; Yoshida, Makoto
    • Applied and Environmental Microbiology, Vol. 85, Issue 24
    • DOI: 10.1128/aem.01692-19

    Influence of Lytic Polysaccharide Monooxygenase Active Site Segments on Activity and Affinity
    journal, December 2019

    • Laurent, Christophe V. F. P.; Sun, Peicheng; Scheiblbrandner, Stefan
    • International Journal of Molecular Sciences, Vol. 20, Issue 24
    • DOI: 10.3390/ijms20246219

    Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose
    journal, June 2016

    • Garajova, Sona; Mathieu, Yann; Beccia, Maria Rosa
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep28276

    Lytic polysaccharide monooxygenases and other oxidative enzymes are abundantly secreted by Aspergillus nidulans grown on different starches
    journal, September 2016

    • Nekiunaite, Laura; Arntzen, Magnus Ø.; Svensson, Birte
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0604-0

    Molecular mechanism of lytic polysaccharide monooxygenases
    journal, January 2018

    • Hedegård, Erik Donovan; Ryde, Ulf
    • Chemical Science, Vol. 9, Issue 15
    • DOI: 10.1039/c8sc00426a

    Salt-responsive lytic polysaccharide monooxygenases from the mangrove fungus Pestalotiopsis sp. NCi6
    journal, May 2016

    Interactions of a fungal lytic polysaccharide monooxygenase with β-glucan substrates and cellobiose dehydrogenase
    journal, May 2016

    • Courtade, Gaston; Wimmer, Reinhard; Røhr, Åsmund K.
    • Proceedings of the National Academy of Sciences, Vol. 113, Issue 21
    • DOI: 10.1073/pnas.1602566113

    Direct Electron Transfer of Enzymes Facilitated by Cytochromes
    journal, December 2018

    X-ray structure of the direct electron transfer-type FAD glucose dehydrogenase catalytic subunit complexed with a hitchhiker protein
    journal, August 2019

    • Yoshida, Hiromi; Kojima, Katsuhiro; Shiota, Masaki
    • Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 9
    • DOI: 10.1107/s2059798319010878

    Influence of Lytic Polysaccharide Monooxygenase Active Site Segments on Activity and Affinity
    journal, December 2019

    • Laurent, Christophe V. F. P.; Sun, Peicheng; Scheiblbrandner, Stefan
    • International Journal of Molecular Sciences, Vol. 20, Issue 24
    • DOI: 10.3390/ijms20246219

    Lytic polysaccharide monooxygenases from Myceliophthora thermophila C1 differ in substrate preference and reducing agent specificity
    journal, August 2016

    • Frommhagen, Matthias; Koetsier, Martijn J.; Westphal, Adrie H.
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0594-y
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