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

Motycka, Bettina; Csarman, Florian; Rupp, Melanie; Schnabel, Karoline; Nagy, Gabor; Karnpakdee, Kwankao; Scheiblbrandner, Stefan; Tscheliessnig, Rupert; Oostenbrink, Chris; Hammel, Michal; Ludwig, Roland

doi:10.1002/cbic.202300431

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

Journal Article · Thu Sep 28 00:00:00 EDT 2023 · ChemBioChem: a European journal of chemical biology

DOI:https://doi.org/10.1002/cbic.202300431· OSTI ID:2280921

^[1]; ^[2]; ^[2]; Schnabel, Karoline ^[2]; ^[3]; ^[2]; ^[2]; ^[4]; ^[2]; ^[5]; ^[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)
Max Planck Institute for Multidisciplinary Sciences (Germany)
Univ. of Natural Resources and Life Sciences, Vienna (Austria); Medical University of Graz (Austria)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

The function of cellobiose dehydrogenase (CDH) in biosensors, biofuel cells, and as a physiological redox partner of lytic polysaccharide monooxygenase (LPMO) is based on its role as an electron donor. Before donating electrons to LPMO or electrodes, an interdomain electron transfer from the catalytic FAD-containing dehydrogenase domain to the electron shuttling cytochrome domain of CDH is required. This study investigates the role of two crucial amino acids located at the dehydrogenase domain on domain interaction and interdomain electron transfer by structure-based engineering. The electron transfer kinetics of wild-type Myriococcum thermophilum CDH and its variants M309A, R698S, and M309A/R698S were analyzed by stopped-flow spectrophotometry and structural effects were studied by small-angle X-ray scattering. The data show that R698 is essential to pull the cytochrome domain close to the dehydrogenase domain and orient the heme propionate group towards the FAD, while M309 is an integral part of the electron transfer pathway – its mutation reducing the interdomain electron transfer 10-fold. Structural models and molecular dynamics simulations pinpoint the action of these two residues on the domain interaction and interdomain electron transfer.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2280921

Journal Information:: ChemBioChem: a European journal of chemical biology, Journal Name: ChemBioChem: a European journal of chemical biology Journal Issue: 22 Vol. 24; ISSN 1439-4227

Publisher:: ChemPubSoc EuropeCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

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
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
Molecular dynamics simulations give insight into the conformational change, complex formation, and electron transfer pathway for cytochrome P450 reductase: MD Simulations on Cytochrome P450 Reductase Sündermann, Axel; Oostenbrink, Chris Protein Science, Vol. 22, Issue 9 https://doi.org/10.1002/pro.2307	journal	August 2013
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
Cellobiose dehydrogenase modified electrodes: advances by materials science and biochemical engineering Ludwig, Roland; Ortiz, Roberto; Schulz, Christopher Analytical and Bioanalytical Chemistry, Vol. 405, Issue 11 https://doi.org/10.1007/s00216-012-6627-x	journal	January 2013
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
Cellobiose dehydrogenase is essential for wood invasion and nonessential for kraft pulp delignification by Trametes versicolor Dumonceaux, Tim; Bartholomew, Kirk; Valeanu, Loredana Enzyme and Microbial Technology, Vol. 29, Issue 8-9 https://doi.org/10.1016/S0141-0229(01)00407-0	journal	November 2001
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
Agaricus meleagris pyranose dehydrogenase: Influence of covalent FAD linkage on catalysis and stability Krondorfer, Iris; Brugger, Dagmar; Paukner, Regina Archives of Biochemistry and Biophysics, Vol. 558 https://doi.org/10.1016/j.abb.2014.07.008	journal	September 2014
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
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
Architecture, implementation and parallelisation of the GROMOS software for biomolecular simulation Schmid, Nathan; Christ, Clara D.; Christen, Markus Computer Physics Communications, Vol. 183, Issue 4 https://doi.org/10.1016/j.cpc.2011.12.014	journal	April 2012
Protein Conformational Change Is Essential for Reductive Activation of Lytic Polysaccharide Monooxygenase by Cellobiose Dehydrogenase Breslmayr, Erik; Laurent, Christophe V. F. P.; Scheiblbrandner, Stefan ACS Catalysis, Vol. 10, Issue 9 https://doi.org/10.1021/acscatal.0c00754	journal	March 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
Redox Control of the Catalytic Cycle of Flavocytochrome P-450 BM3 Daff, S. N.; Chapman, S. K. Biochemistry, Vol. 36, Issue 45 https://doi.org/10.1021/bi971085s	journal	November 1997
GROMOS++ Software for the Analysis of Biomolecular Simulation Trajectories Eichenberger, Andreas P.; Allison, Jane R.; Dolenc, Jožica Journal of Chemical Theory and Computation, Vol. 7, Issue 10 https://doi.org/10.1021/ct2003622	journal	September 2011
New Interaction Parameters for Charged Amino Acid Side Chains in the GROMOS Force Field Reif, Maria M.; Hünenberger, Philippe H.; Oostenbrink, Chris Journal of Chemical Theory and Computation, Vol. 8, Issue 10 https://doi.org/10.1021/ct300156h	journal	March 2012
Electron tunneling pathways in ruthenated proteins Beratan, David N.; Onuchic, Jose Nelson; Betts, Jonathan N. Journal of the American Chemical Society, Vol. 112, Issue 22 https://doi.org/10.1021/ja00178a011	journal	October 1990
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
Sustainable bioenergy production from marginal lands in the US Midwest Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong Nature, Vol. 493, Issue 7433 https://doi.org/10.1038/nature11811	journal	January 2013
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
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
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
Comprehensive macromolecular conformations mapped by quantitative SAXS analyses Hura, Greg L.; Budworth, Helen; Dyer, Kevin N. Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2453	journal	April 2013
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
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
Electron transfer chain reaction of the extracellular flavocytochrome cellobiose dehydrogenase from the basidiomycete Phanerochaete chrysosporium: Electron transfer chain reaction of CDH Igarashi, Kiyohiko; Yoshida, Makoto; Matsumura, Hirotoshi FEBS Journal, Vol. 272, Issue 11 https://doi.org/10.1111/j.1742-4658.2005.04707.x	journal	May 2005
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
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J. Science, Vol. 330, Issue 6001, p. 219-222 https://doi.org/10.1126/science.1192231	journal	October 2010
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
The GMC superfamily of oxidoreductases revisited: analysis and evolution of fungal GMC oxidoreductases Sützl, Leander; Foley, Gabriel; Gillam, Elizabeth M. J. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1457-0	journal	May 2019
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

Similar Records

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

Journal Article · Wed Jun 07 20:00:00 EDT 2023 · Federation of European Biochemical Societies (FEBS) Journal · OSTI ID:2473029

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

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

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
cellobiose dehydrogenase
electron transfer
molecular dynamic simulation
multistate modeling
small angle x-ray scattering

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

Citation Formats

References (44)

Similar Records

Related Subjects