Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms

Abstract

Background: Cellobiose dehydrogenases have gained interest due to their potential applications in sectors from biofuel production to biomedical devices. The CDHIIA variant is comprised of a cytochrome domain (CYT), a dehydrogenase domain (DH), and a carbohydrate-binding module (CBM) that are connected by two flexible linkers. Upon cellobiose oxidation at the DH, intramolecular electron transfer (IaET) occurs from the DH to the CYT. In vivo, CDHIIA CYT subsequently performs intermolecular electron transfer (IeET) to a lytic polysaccharide monooxygenase (LPMO). The relevant solution-state CDH domain conformations for IaET and IeET have not been fully characterized.Methods: Small-angle X-ray and neutron scattering measurements of oxidized CDHIIA from Myriococcum thermophilum and Neurospora crassa were performed to investigate the structural landscape explored in solution by MtCDHIIA and NcCDHIIA in response to cations, pH, and the presence of an electron acceptor, LPMO9D from N. crassa.Results: The scattering data complemented by modeling show that, under oxidizing conditions, MtCDHIIA undergoes global conformational rearrangement in the presence of Ca2+. Oxidized NcCDHIIA exhibits conformational changes upon pH variation and, in the presence of NcLPMO9D, primarily adopts a compact conformation.Conclusions: These results demonstrate different conformational responses of oxidized MtCDHIIA and NcCDHIIA to changes in environment. The results also reveal a shift inmore » the oxidized NcCDHIIA conformational landscape toward interdomain compaction upon co-incubation with NcLPMO9D.General significance: The present study is the first report on the structural landscapes explored in solution by oxidized cellobiose dehydrogenases under various cation concentrations, pH conditions and in the presence of an electron-accepting LPMO.« less

Authors:
 [1];  [1];  [2];  [2];  [2];  [1]
+ Show Author Affiliations
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); North Carolina State Univ., Raleigh, NC (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1424446
Alternate Identifier(s):
OSTI ID: 1495295
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Biochimica et Biophysica Acta - General Subjects
Additional Journal Information:
Journal Volume: 1862; Journal Issue: 4; Journal ID: ISSN 0304-4165
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
72 PHYSICS OF ELEMENTARY PARTICLES AND FIELDS; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bodenheimer, Annette M., O'Dell, William B., Oliver, Ryan C., Qian, Shuo, Stanley, Christopher B., and Meilleur, Flora. Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms. United States: N. p., 2018. Web. doi:10.1016/j.bbagen.2018.01.016.
Copy to clipboard
Bodenheimer, Annette M., O'Dell, William B., Oliver, Ryan C., Qian, Shuo, Stanley, Christopher B., & Meilleur, Flora. Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms. United States. https://doi.org/10.1016/j.bbagen.2018.01.016
Copy to clipboard
Bodenheimer, Annette M., O'Dell, William B., Oliver, Ryan C., Qian, Shuo, Stanley, Christopher B., and Meilleur, Flora. Wed . "Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms". United States. https://doi.org/10.1016/j.bbagen.2018.01.016. https://www.osti.gov/servlets/purl/1424446.
Copy to clipboard
@article{osti_1424446,
title = {Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms},
author = {Bodenheimer, Annette M. and O'Dell, William B. and Oliver, Ryan C. and Qian, Shuo and Stanley, Christopher B. and Meilleur, Flora},
abstractNote = {Background: Cellobiose dehydrogenases have gained interest due to their potential applications in sectors from biofuel production to biomedical devices. The CDHIIA variant is comprised of a cytochrome domain (CYT), a dehydrogenase domain (DH), and a carbohydrate-binding module (CBM) that are connected by two flexible linkers. Upon cellobiose oxidation at the DH, intramolecular electron transfer (IaET) occurs from the DH to the CYT. In vivo, CDHIIA CYT subsequently performs intermolecular electron transfer (IeET) to a lytic polysaccharide monooxygenase (LPMO). The relevant solution-state CDH domain conformations for IaET and IeET have not been fully characterized.Methods: Small-angle X-ray and neutron scattering measurements of oxidized CDHIIA from Myriococcum thermophilum and Neurospora crassa were performed to investigate the structural landscape explored in solution by MtCDHIIA and NcCDHIIA in response to cations, pH, and the presence of an electron acceptor, LPMO9D from N. crassa.Results: The scattering data complemented by modeling show that, under oxidizing conditions, MtCDHIIA undergoes global conformational rearrangement in the presence of Ca2+. Oxidized NcCDHIIA exhibits conformational changes upon pH variation and, in the presence of NcLPMO9D, primarily adopts a compact conformation.Conclusions: These results demonstrate different conformational responses of oxidized MtCDHIIA and NcCDHIIA to changes in environment. The results also reveal a shift in the oxidized NcCDHIIA conformational landscape toward interdomain compaction upon co-incubation with NcLPMO9D.General significance: The present study is the first report on the structural landscapes explored in solution by oxidized cellobiose dehydrogenases under various cation concentrations, pH conditions and in the presence of an electron-accepting LPMO.},
doi = {10.1016/j.bbagen.2018.01.016},
journal = {Biochimica et Biophysica Acta - General Subjects},
number = 4,
volume = 1862,
place = {United States},
year = {Wed Jan 31 00:00:00 EST 2018},
month = {Wed Jan 31 00:00:00 EST 2018}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.bbagen.2018.01.016
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: P(r) functions calculated from the NcCDHIIA SANS data are normalized to a maximum height of 1.0 for ease of comparison (pD 5.5, A & B; pD 7.5, C & D).
All figures and tables (8 total)
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Fungal Cellulases
journal, January 2015

  • Payne, Christina M.; Knott, Brandon C.; Mayes, Heather B.
  • Chemical Reviews, Vol. 115, Issue 3
  • DOI: 10.1021/cr500351c

Cellobiose dehydrogenase (cellobiose oxidase) from Phanerochaete chrysosporium as a wood-degrading enzyme. Studies on cellulose, xylan and synthetic lignin
journal, January 1995

  • Henriksson, G.; Ander, P.; Pettersson, B.
  • Applied Microbiology and Biotechnology, Vol. 42, Issue 5
  • DOI: 10.1007/BF00171963

Catalytic Properties and Classification of Cellobiose Dehydrogenases from Ascomycetes
journal, March 2011

  • Harreither, Wolfgang; Sygmund, Christoph; Augustin, Manfred
  • Applied and Environmental Microbiology, Vol. 77, Issue 5
  • DOI: 10.1128/AEM.02052-10

Quantitative Proteomic Approach for Cellulose Degradation by Neurospora crassa
journal, September 2011

  • Phillips, Christopher M.; Iavarone, Anthony T.; Marletta, Michael A.
  • Journal of Proteome Research, Vol. 10, Issue 9
  • DOI: 10.1021/pr200329b

Carbohydrate-dependent Enzymic Quinone Reduction during Lignin Degradation.
journal, January 1974

Cellobiose:Quinone Oxidoreductase, a New Wood-degrading Enzyme from White-rot Fungi.
journal, January 1974

Purification and Properties of Cellobiose:Quinone Oxidoreductase from Sporotrichum pulverulentum.
journal, January 1975

A new scaffold for binding haem in the cytochrome domain of the extracellular flavocytochrome cellobiose dehydrogenase
journal, January 2000

Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase
journal, January 2002

  • Martin Hallberg, B.; Henriksson, Gunnar; Pettersson, Göran
  • Journal of Molecular Biology, Vol. 315, Issue 3
  • DOI: 10.1006/jmbi.2001.5246

Mechanism of the Reductive Half-reaction in Cellobiose Dehydrogenase
journal, December 2002

  • Hallberg, B. Martin; Henriksson, Gunnar; Pettersson, Göran
  • Journal of Biological Chemistry, Vol. 278, Issue 9
  • DOI: 10.1074/jbc.M210961200

Interdomain flip-flop motion visualized in flavocytochrome cellobiose dehydrogenase using high-speed atomic force microscopy during catalysis
journal, January 2017

  • Harada, Hirofumi; Onoda, Akira; Uchihashi, Takayuki
  • Chemical Science, Vol. 8, Issue 9
  • DOI: 10.1039/C7SC01672G

Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation
journal, July 2015

  • Tan, Tien-Chye; Kracher, Daniel; Gandini, Rosaria
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms8542

Cellobiose Dehydrogenase – A Flavocytochrome from Wood-Degrading, Phytopathogenic and Saprotropic Fungi
journal, June 2006

Natural engineering principles of electron tunnelling in biological oxidation–reduction
journal, November 1999

  • Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi
  • Nature, Vol. 402, Issue 6757
  • DOI: 10.1038/46972

A novel bio-electronic tongue using different cellobiose dehydrogenases to resolve mixtures of various sugars and interfering analytes
journal, May 2016

Antimicrobial Cellobiose Dehydrogenase-Chitosan Particles
journal, December 2015

  • Tegl, Gregor; Thallinger, Barbara; Beer, Bianca
  • ACS Applied Materials & Interfaces, Vol. 8, Issue 1
  • DOI: 10.1021/acsami.5b10801

Preventing microbial colonisation of catheters: Antimicrobial and antibiofilm activities of cellobiose dehydrogenase
journal, November 2014

Investigation of Graphite Electrodes Modified with Cellobiose Dehydrogenase from the AscomyceteMyriococcum thermophilum
journal, January 2007

  • Harreither, Wolfgang; Coman, Vasile; Ludwig, Roland
  • Electroanalysis, Vol. 19, Issue 2-3
  • DOI: 10.1002/elan.200603688

Inter‐domain electron transfer in cellobiose dehydrogenase: modulation by pH and divalent cations
journal, May 2015

  • Kracher, Daniel; Zahma, Kawah; Schulz, Christopher
  • The FEBS Journal, Vol. 282, Issue 16
  • DOI: 10.1111/febs.13310

Enhancement of enzymatic activity and catalytic current of cellobiose dehydrogenase by calcium ions
journal, April 2012

Structural Basis for Substrate Targeting and Catalysis by Fungal Polysaccharide Monooxygenases
journal, June 2012

  • Li, Xin; Beeson, William T.; Phillips, Christopher M.
  • Structure, Vol. 20, Issue 6, p. 1051-1061
  • DOI: 10.1016/j.str.2012.04.002

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

Structural studies of Neurospora crassa LPMO9D and redox partner CDHIIA using neutron crystallography and small-angle scattering
journal, August 2017

Domain Motion in Cytochrome P450 Reductase: CONFORMATIONAL EQUILIBRIA REVEALED BY NMR AND SMALL-ANGLE X-RAY SCATTERING
journal, October 2009

  • Ellis, Jacqueline; Gutierrez, Aldo; Barsukov, Igor L.
  • Journal of Biological Chemistry, Vol. 284, Issue 52
  • DOI: 10.1074/jbc.M109.054304

Redox-Linked Domain Movements in the Catalytic Cycle of Cytochrome P450 Reductase
journal, September 2013

ACIDITY MEASUREMENTS WITH THE GLASS ELECTRODE IN H 2 O-D 2 O MIXTURES
journal, May 1960

  • Mikkelsen, Kirsten; Nielsen, Sigurd Olaf
  • The Journal of Physical Chemistry, Vol. 64, Issue 5
  • DOI: 10.1021/j100834a026

Accurate assessment of mass, models and resolution by small-angle scattering
journal, April 2013

Determination of the regularization parameter in indirect-transform methods using perceptual criteria
journal, August 1992

Investigation of the pH-Dependent Electron Transfer Mechanism of Ascomycetous Class II Cellobiose Dehydrogenases on Electrodes
journal, April 2012

  • Harreither, Wolfgang; Nicholls, Peter; Sygmund, Christoph
  • Langmuir, Vol. 28, Issue 16
  • DOI: 10.1021/la3005486

Structural insight into the calcium ion modulated interdomain electron transfer in cellobiose dehydrogenase
journal, April 2015

Interdomain electron transfer in cellobiose dehydrogenase is governed by surface electrostatics
journal, February 2017

  • Kadek, Alan; Kavan, Daniel; Marcoux, Julien
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1861, Issue 2
  • DOI: 10.1016/j.bbagen.2016.11.016

Characterization of the Two Neurospora crassa Cellobiose Dehydrogenases and Their Connection to Oxidative Cellulose Degradation
journal, June 2012

  • Sygmund, Christoph; Kracher, Daniel; Scheiblbrandner, Stefan
  • Applied and Environmental Microbiology, Vol. 78, Issue 17
  • DOI: 10.1128/AEM.01503-12

Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase
journal, December 2016

  • O'Dell, William B.; Agarwal, Pratul K.; Meilleur, Flora
  • Angewandte Chemie International Edition, Vol. 56, Issue 3
  • DOI: 10.1002/anie.201610502

The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory
journal, June 2014

  • Heller, William T.; Urban, Volker S.; Lynn, Gary W.
  • Journal of Applied Crystallography, Vol. 47, Issue 4
  • DOI: 10.1107/S1600576714011285

Mantid—Data analysis and visualization package for neutron scattering and μ SR experiments
journal, November 2014

  • Arnold, O.; Bilheux, J. C.; Borreguero, J. M.
  • Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764
  • DOI: 10.1016/j.nima.2014.07.029

PRIMUS: a Windows PC-based system for small-angle scattering data analysis
journal, September 2003

  • Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V.
  • Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282
  • DOI: 10.1107/S0021889803012779

FoXS, FoXSDock and MultiFoXS: Single-state and multi-state structural modeling of proteins and their complexes based on SAXS profiles
journal, May 2016

  • Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A.
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw389

CHARMM-GUI: A web-based graphical user interface for CHARMM
journal, March 2008

  • Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G.
  • Journal of Computational Chemistry, Vol. 29, Issue 11
  • DOI: 10.1002/jcc.20945

Glycan reader: Automated sugar identification and simulation preparation for carbohydrates and glycoproteins
journal, August 2011

  • Jo, Sunhwan; Song, Kevin C.; Desaire, Heather
  • Journal of Computational Chemistry, Vol. 32, Issue 14
  • DOI: 10.1002/jcc.21886

SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints
journal, February 2012

  • Curtis, Joseph E.; Raghunandan, Sindhu; Nanda, Hirsh
  • Computer Physics Communications, Vol. 183, Issue 2
  • DOI: 10.1016/j.cpc.2011.09.010

Small-angle X-ray scattering studies on cellobiose dehydrogenase from Phanerochaete chrysosporium
journal, March 1996

  • Lehner, Dieter; Zipper, Peter; Henriksson, Gunnar
  • Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1293, Issue 1
  • DOI: 10.1016/0167-4838(95)00245-6

The extended Q -range small-angle neutron scattering diffractometer at the SNS
journal, July 2010

UCSF Chimera, MODELLER, and IMP: An integrated modeling system
journal, September 2012

  • Yang, Zheng; Lasker, Keren; Schneidman-Duhovny, Dina
  • Journal of Structural Biology, Vol. 179, Issue 3
  • DOI: 10.1016/j.jsb.2011.09.006
    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

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

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

      Sort by:
      [ × clear filter / sort ]

      Figures / Tables found in this record:

      Fig. 1 (p. 3)figure
      Fig. 2 (p. 3)figure
      Fig. 3 (p. 4)figure
      Table 1 (p. 5)table
      Fig. 4 (p. 6)figure
      Fig. 5 (p. 7)figure
      Fig. 6 (p. 7)figure
      Table 2 (p. 7)table
        [ × clear filter / sort ]
        Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

        Similar Records in DOE PAGES and OSTI.GOV collections: