Resolving domain positions of cellobiose dehydrogenase by small angle X–ray scattering

Motycka, Bettina; Csarman, Florian; Tscheliessnig, Rupert; Hammel, Michal; Ludwig, Roland

doi:10.1111/febs.16885

Resolving domain positions of cellobiose dehydrogenase by small angle X–ray scattering

Journal Article · Thu Jun 08 00:00:00 EDT 2023 · Federation of European Biochemical Societies (FEBS) Journal

DOI:https://doi.org/10.1111/febs.16885· OSTI ID:2473029

Motycka, Bettina ^[1]; ^[2]; Tscheliessnig, Rupert ^[3]; Hammel, Michal ^[4]; ^[2]

Univ. of Natural Resources and Life Sciences, Vienna (Austria); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of Natural Resources and Life Sciences, Vienna (Austria)
Univ. of Natural Resources and Life Sciences, Vienna (Austria); Medical University of Graz (Austria)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

The interdomain electron transfer (IET) between the catalytic flavodehydrogenase domain and the electron-transferring cytochrome domain of cellobiose dehydrogenase (CDH) plays an essential role in biocatalysis, biosensors and biofuel cells, as well as in its natural function as an auxiliary enzyme of lytic polysaccharide monooxygenase. We investigated the mobility of the cytochrome and dehydrogenase domains of CDH, which is hypothesised to limit IET in solution by small angle X-ray scattering (SAXS). CDH from Myriococcum thermophilum (syn. Crassicarpon hotsonii, syn. Thermothelomyces myriococcoides) was probed by SAXS to study the CDH mobility at different pH and in the presence of divalent cations. By comparison of the experimental SAXS data, using pair-distance distribution functions and Kratky plots, we show an increase in CDH mobility at higher pH, indicating alterations of domain mobility. To further visualise CDH movement in solution, we performed SAXS-based multistate modelling. Glycan structures present on CDH partially masked the resulting SAXS shapes, we diminished these effects by deglycosylation and studied the effect of glycoforms by modelling. The modelling shows that with increasing pH, the cytochrome domain adopts a more flexible state with significant separation from the dehydrogenase domain. On the contrary, the presence of calcium ions decreases the mobility of the cytochrome domain. Experimental SAXS data, multistate modelling and previously reported kinetic data show how pH and divalent ions impact the closed state necessary for the IET governed by the movement of the CDH cytochrome domain.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Austrian Science Fund (FWF); National Cancer Institute (NCI); National Institute of General Medical Sciences (NIGMS); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2473029

Journal Information:: Federation of European Biochemical Societies (FEBS) Journal, Journal Name: Federation of European Biochemical Societies (FEBS) Journal Journal Issue: 19 Vol. 290; ISSN 1742-464X

Publisher:: Federation of European Biochemical SocietiesCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

Investigation of Graphite Electrodes Modified with Cellobiose Dehydrogenase from the AscomyceteMyriococcum thermophilum Harreither, Wolfgang; Coman, Vasile; Ludwig, Roland Electroanalysis, Vol. 19, Issue 2-3 https://doi.org/10.1002/elan.200603688	journal	January 2007
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase Martin Hallberg, B.; Henriksson, Gunnar; Pettersson, Göran Journal of Molecular Biology, Vol. 315, Issue 3 https://doi.org/10.1006/jmbi.2001.5246	journal	January 2002
Modeling Structure and Dynamics of Protein Complexes with SAXS Profiles Schneidman-Duhovny, Dina; Hammel, Michal Protein Complex Assembly https://doi.org/10.1007/978-1-4939-7759-8_29	book	January 2018
Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS) Hammel, Michal European Biophysics Journal, Vol. 41, Issue 10 https://doi.org/10.1007/s00249-012-0820-x	journal	May 2012
Cellobiose oxidase of Phanerochaete chrysosporium enhances crystalline cellulose degradation by cellulases Bao, Wenjun; Renganathan, V. FEBS Letters, Vol. 302, Issue 1 https://doi.org/10.1016/0014-5793(92)80289-S	journal	May 1992
Small-angle X-ray scattering studies on cellobiose dehydrogenase from Phanerochaete chrysosporium Lehner, Dieter; Zipper, Peter; Henriksson, Gunnar Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1293, Issue 1 https://doi.org/10.1016/0167-4838(95)00245-6	journal	March 1996
Is cellobiose dehydrogenase from Phanerochaete chrysosporium a lignin degrading enzyme? Henriksson, Gunnar; Zhang, Liming; Li, Jiebing Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1480, Issue 1-2 https://doi.org/10.1016/S0167-4838(00)00096-0	journal	July 2000
Size exclusion chromatography coupled small angle X-ray scattering with tandem multiangle light scattering at the SIBYLS beamline Rosenberg, Daniel J.; Hura, Greg L.; Hammel, Michal Small Angle Scattering Part A: Methods for Structural Investigation https://doi.org/10.1016/bs.mie.2022.08.031	book	January 2022
Interdomain electron transfer in cellobiose dehydrogenase is governed by surface electrostatics Kadek, Alan; Kavan, Daniel; Marcoux, Julien Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1861, Issue 2 https://doi.org/10.1016/j.bbagen.2016.11.016	journal	February 2017
Structural investigation of cellobiose dehydrogenase IIA: Insights from small angle scattering into intra- and intermolecular electron transfer mechanisms Bodenheimer, Annette M.; O'Dell, William B.; Oliver, Ryan C. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1862, Issue 4 https://doi.org/10.1016/j.bbagen.2018.01.016	journal	April 2018
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Structural studies of Neurospora crassa LPMO9D and redox partner CDHIIA using neutron crystallography and small-angle scattering Bodenheimer, Annette M.; O'Dell, William B.; Stanley, Christopher B. Carbohydrate Research, Vol. 448 https://doi.org/10.1016/j.carres.2017.03.001	journal	August 2017
Lignocellulose degradation mechanisms across the Tree of Life Cragg, Simon M.; Beckham, Gregg T.; Bruce, Neil C. Current Opinion in Chemical Biology, Vol. 29 https://doi.org/10.1016/j.cbpa.2015.10.018	journal	December 2015
Structural characterization of proteins and complexes using small-angle X-ray solution scattering Mertens, Haydyn D. T.; Svergun, Dmitri I. Journal of Structural Biology, Vol. 172, Issue 1 https://doi.org/10.1016/j.jsb.2010.06.012	journal	October 2010
X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Putnam, Christopher D.; Hammel, Michal; Hura, Greg L. Quarterly Reviews of Biophysics, Vol. 40, Issue 3 https://doi.org/10.1017/S0033583507004635	journal	August 2007
Determination of the Distance Between the Cytochrome and Dehydrogenase Domains of Immobilized Cellobiose Dehydrogenase by Using Surface Plasmon Resonance with a Center of Mass Based Model Tuoriniemi, Jani; Gorton, Lo; Ludwig, Roland Analytical Chemistry, Vol. 92, Issue 3 https://doi.org/10.1021/acs.analchem.9b04490	journal	January 2020
Predicting the Structures of Glycans, Glycoproteins, and Their Complexes Woods, Robert J. Chemical Reviews, Vol. 118, Issue 17 https://doi.org/10.1021/acs.chemrev.8b00032	journal	June 2018
Chimeric Cellobiose Dehydrogenases Reveal the Function of Cytochrome Domain Mobility for the Electron Transfer to Lytic Polysaccharide Monooxygenase Felice, Alfons K. G.; Schuster, Christian; Kadek, Alan ACS Catalysis, Vol. 11, Issue 2 https://doi.org/10.1021/acscatal.0c05294	journal	December 2020
Direct Electron-Transfer Anisotropy of a Site-Specifically Immobilized Cellobiose Dehydrogenase Ma, Su; Laurent, Christophe V. F. P.; Meneghello, Marta ACS Catalysis, Vol. 9, Issue 8 https://doi.org/10.1021/acscatal.9b02014	journal	July 2019
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family Harris, Paul; Welner, Ditte; McFarland, K. Biochemistry, Vol. 49, Issue 15, p. 3305-3316 https://doi.org/10.1021/bi100009p	journal	April 2010
Oxidative Cleavage of Cellulose by Fungal Copper-Dependent Polysaccharide Monooxygenases Beeson, William T.; Phillips, Christopher M.; Cate, Jamie H. D. Journal of the American Chemical Society, Vol. 134, Issue 2 https://doi.org/10.1021/ja210657t	journal	December 2011
Natural engineering principles of electron tunnelling in biological oxidation–reduction Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi Nature, Vol. 402, Issue 6757 https://doi.org/10.1038/46972	journal	November 1999
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation Tan, Tien-Chye; Kracher, Daniel; Gandini, Rosaria Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8542	journal	July 2015
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
Interdomain flip-flop motion visualized in flavocytochrome cellobiose dehydrogenase using high-speed atomic force microscopy during catalysis Harada, Hirofumi; Onoda, Akira; Uchihashi, Takayuki Chemical Science, Vol. 8, Issue 9 https://doi.org/10.1039/C7SC01672G	journal	January 2017
Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa Tian, Chaoguang; Beeson, William T.; Iavarone, Anthony T. Proceedings of the National Academy of Sciences, Vol. 106, Issue 52 https://doi.org/10.1073/pnas.0906810106	journal	December 2009
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
Cellulose Surface Degradation by a Lytic Polysaccharide Monooxygenase and Its Effect on Cellulase Hydrolytic Efficiency Eibinger, Manuel; Ganner, Thomas; Bubner, Patricia Journal of Biological Chemistry, Vol. 289, Issue 52 https://doi.org/10.1074/jbc.M114.602227	journal	October 2014
FoXS, FoXSDock and MultiFoXS: Single-state and multi-state structural modeling of proteins and their complexes based on SAXS profiles Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw389	journal	May 2016
SWISS-MODEL: homology modelling of protein structures and complexes Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky427	journal	May 2018
Implementation and performance of SIBYLS: a dual endstation small-angle X-ray scattering and macromolecular crystallography beamline at the Advanced Light Source Classen, Scott; Hura, Greg L.; Holton, James M. Journal of Applied Crystallography, Vol. 46, Issue 1 https://doi.org/10.1107/S0021889812048698	journal	January 2013
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
BioXTAS RAW : improvements to a free open-source program for small-angle X-ray scattering data reduction and analysis Hopkins, Jesse Bennett; Gillilan, Richard E.; Skou, Soren Journal of Applied Crystallography, Vol. 50, Issue 5 https://doi.org/10.1107/S1600576717011438	journal	September 2017
Inter‐domain electron transfer in cellobiose dehydrogenase: modulation by pH and divalent cations Kracher, Daniel; Zahma, Kawah; Schulz, Christopher The FEBS Journal, Vol. 282, Issue 16 https://doi.org/10.1111/febs.13310	journal	May 2015
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
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Characterization of the Two Neurospora crassa Cellobiose Dehydrogenases and Their Connection to Oxidative Cellulose Degradation Sygmund, Christoph; Kracher, Daniel; Scheiblbrandner, Stefan Applied and Environmental Microbiology, Vol. 78, Issue 17 https://doi.org/10.1128/AEM.01503-12	journal	June 2012
Catalytic Properties and Classification of Cellobiose Dehydrogenases from Ascomycetes Harreither, Wolfgang; Sygmund, Christoph; Augustin, Manfred Applied and Environmental Microbiology, Vol. 77, Issue 5 https://doi.org/10.1128/AEM.02052-10	journal	March 2011
Purification and Characterization of Cellobiose Dehydrogenase from the Plant PathogenSclerotium(Athelia)rolfsii Baminger, Ursula; Subramaniam, Sai S.; Renganathan, V. Applied and Environmental Microbiology, Vol. 67, Issue 4 https://doi.org/10.1128/AEM.67.4.1766-1774.2001	journal	April 2001
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Cellobiose Dehydrogenase – A Flavocytochrome from Wood-Degrading, Phytopathogenic and Saprotropic Fungi Zamocky, Marcel; Ludwig, R.; Peterbauer, C. Current Protein & Peptide Science, Vol. 7, Issue 3 https://doi.org/10.2174/138920306777452367	journal	June 2006
Structure and flexibility within proteins as identified through small angle X-ray scattering Pelikan, M.; Hura, G.; Hammel, M. General Physiology and Biophysics, Vol. 28, Issue 2 https://doi.org/10.4149/gpb_2009_02_174	journal	January 2009
Production platforms for biotherapeutic glycoproteins. Occurrence, impact, and challenges of non-human sialylation Ghaderi, Darius; Zhang, Mai; Hurtado-Ziola, Nancy Biotechnology and Genetic Engineering Reviews, Vol. 28, Issue 1 https://doi.org/10.5661/bger-28-147	journal	January 2012

Similar Records

Amino Acid Residues Controlling Domain Interaction and Interdomain Electron Transfer in Cellobiose Dehydrogenase

Journal Article · Wed Sep 27 20:00:00 EDT 2023 · ChemBioChem: a European journal of chemical biology · OSTI ID:2280921

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

Journal Article · Tue Jan 30 19:00:00 EST 2018 · Biochimica et Biophysica Acta - General Subjects · OSTI ID:1424446

Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation

Journal Article · Mon Jul 06 20:00:00 EDT 2015 · Nature Communications · OSTI ID:1623985

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
cellobiose dehydrogenase
conformational changes
interdomain electron transfer
multistate modelling
small angle X-ray scattering

Resolving domain positions of cellobiose dehydrogenase by small angle X–ray scattering

Citation Formats

References (46)

Similar Records

Related Subjects