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.; Meilleur, Flora

doi:10.1016/j.carres.2017.03.001

Title: Structural studies of Neurospora crassa LPMO9D and redox partner CDHIIA using neutron crystallography and small-angle scattering

Journal Article · Sat Mar 04 00:00:00 EST 2017 · Carbohydrate Research

DOI:https://doi.org/10.1016/j.carres.2017.03.001· OSTI ID:1424447

Bodenheimer, Annette M. ^[1];

^[1]; Stanley, Christopher B. ^[2]; Meilleur, Flora ^[1]

North Carolina State Univ., Raleigh, NC (United States). Dept. of Molecular and Structural Biochemistry; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate

Sensitivity to hydrogen/deuterium and lack of observable radiation damage makes cold neutrons an ideal probe the structural studies of proteins with highly photosensitive groups such as the copper center of lytic polysaccharide monooxygenases (LPMOs) and flavin adenine dinucleotide (FAD) and heme redox cofactors of cellobiose dehydrogenases (CDHs). In this paper, neutron crystallography and small-angle neutron scattering are used to investigate Neurospora crassa LPMO9D (NcLPMO9D) and CDHIIA (NcCDHIIA), respectively. The presence of LPMO greatly enhances the efficiency of commercial glycoside hydrolase cocktails in the depolymerization of cellulose. LPMOs can receive electrons from CDHs to activate molecular dioxygen for the oxidation of cellulose resulting in chain cleavage and disruption of local crystallinity. Using neutron protein crystallography, the hydrogen/deuterium atoms of NcLPMO9D could be located throughout the structure. At the copper active site, the protonation states of the side chains of His1, His84, His157 and Tyr168, and the orientation of water molecules could be determined. Small-angle neutron scattering measurements provided low resolution models of NcCDHIIA with both the dehydrogenase and cytochrome domains in oxidized states that exhibited elongated conformations. Finally, this work demonstrates the suitability of neutron diffraction and scattering for characterizing enzymes critical to oxidative cellulose deconstruction.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); North Carolina State University, Raleigh, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); USDA National Inst. of Food and Agriculture (NIFA)

Grant/Contract Number:: AC05-00OR22725; MRI 09229719; IGERT1069091; 1010523

OSTI ID:: 1424447

Alternate ID(s):: OSTI ID: 1576621

Journal Information:: Carbohydrate Research, Vol. 448; ISSN 0008-6215

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 12 works

Citation information provided by
Web of Science

References (33)

Novel enzymes for the degradation of cellulose Horn, Svein; Vaaje-Kolstad, Gustav; Westereng, Bjørge Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 45 https://doi.org/10.1186/1754-6834-5-45	journal	January 2012
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
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
Cellulose Degradation by Polysaccharide Monooxygenases Beeson, William T.; Vu, Van V.; Span, Elise A. Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034439	journal	June 2015
Cellobiose Dehydrogenase: A Versatile Catalyst for Electrochemical Applications Ludwig, Roland; Harreither, Wolfgang; Tasca, Federico ChemPhysChem, Vol. 11, Issue 13 https://doi.org/10.1002/cphc.201000216	journal	July 2010
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
Photoreduction of the active site of the metalloprotein putidaredoxin by synchrotron radiation Corbett, Mary C.; Latimer, Matthew J.; Poulos, Thomas L. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 9 https://doi.org/10.1107/S0907444907035160	journal	August 2007
Towards accurate structural characterization of metal centres in protein crystals: the structures of Ni and Cu T ₆ bovine insulin derivatives Frankaer, Christian Grundahl; Mossin, Susanne; Ståhl, Kenny Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 1 https://doi.org/10.1107/S1399004713029040	journal	December 2013
Structural and Electronic Snapshots during the Transition from a Cu(II) to Cu(I) Metal Center of a Lytic Polysaccharide Monooxygenase by X-ray Photoreduction Gudmundsson, Mikael; Kim, Seonah; Wu, Miao Journal of Biological Chemistry, Vol. 289, Issue 27, p. 18782-18792 https://doi.org/10.1074/jbc.M114.563494	journal	May 2014
Lytic polysaccharide monooxygenases: a crystallographer's view on a new class of biomass-degrading enzymes Frandsen, Kristian E. H.; Lo Leggio, Leila IUCrJ, Vol. 3, Issue 6 https://doi.org/10.1107/S2052252516014147	journal	October 2016
Limiting radiation damage for high-brilliance biological solution scattering: practical experience at the EMBL P12 beamline PETRAIII Jeffries, Cy M.; Graewert, Melissa A.; Svergun, Dmitri I. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577515000375	journal	February 2015
Radiation damage to a protein solution, detected by synchrotron X-ray small-angle scattering: dose-related considerations and suppression by cryoprotectants Kuwamoto, Shigeo; Akiyama, Shuji; Fujisawa, Tetsuro Journal of Synchrotron Radiation, Vol. 11, Issue 6 https://doi.org/10.1107/S0909049504019272	journal	October 2004
Domain Motion in Cytochrome P450 Reductase: CONFORMATIONAL EQUILIBRIA REVEALED BY NMR AND SMALL-ANGLE X-RAY SCATTERING Ellis, Jacqueline; Gutierrez, Aldo; Barsukov, Igor L. Journal of Biological Chemistry, Vol. 284, Issue 52 https://doi.org/10.1074/jbc.M109.054304	journal	October 2009
Redox-Linked Domain Movements in the Catalytic Cycle of Cytochrome P450 Reductase Huang, Wei-Cheng; Ellis, Jacqueline; Moody, Peter C. E. Structure, Vol. 21, Issue 9 https://doi.org/10.1016/j.str.2013.06.022	journal	September 2013
Neutron protein crystallography: A complementary tool for locating hydrogens in proteins O'Dell, William B.; Bodenheimer, Annette M.; Meilleur, Flora Archives of Biochemistry and Biophysics, Vol. 602 https://doi.org/10.1016/j.abb.2015.11.033	journal	July 2016
Crystallization of a fungal lytic polysaccharide monooxygenase expressed from glycoengineered Pichia pastoris for X-ray and neutron diffraction O'Dell, William B.; Swartz, Paul D.; Weiss, Kevin L. Acta Crystallographica Section F Structural Biology Communications, Vol. 73, Issue 2 https://doi.org/10.1107/S2053230X16020318	journal	January 2017
On the catalytic mechanisms of lytic polysaccharide monooxygenases Walton, Paul H.; Davies, Gideon J. Current Opinion in Chemical Biology, Vol. 31 https://doi.org/10.1016/j.cbpa.2016.04.001	journal	April 2016
The Copper Active Site of CBM33 Polysaccharide Oxygenases Hemsworth, Glyn R.; Taylor, Edward J.; Kim, Robbert Q. Journal of the American Chemical Society, Vol. 135, Issue 16 https://doi.org/10.1021/ja402106e	journal	April 2013
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
The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases Frandsen, Kristian E. H.; Simmons, Thomas J.; Dupree, Paul Nature Chemical Biology, Vol. 12, Issue 4 https://doi.org/10.1038/nchembio.2029	journal	February 2016
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
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
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
SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints Curtis, Joseph E.; Raghunandan, Sindhu; Nanda, Hirsh Computer Physics Communications, Vol. 183, Issue 2 https://doi.org/10.1016/j.cpc.2011.09.010	journal	February 2012
Enhancement of enzymatic activity and catalytic current of cellobiose dehydrogenase by calcium ions Schulz, Christopher; Ludwig, Roland; Micheelsen, Pernille O. Electrochemistry Communications, Vol. 17 https://doi.org/10.1016/j.elecom.2012.01.031	journal	April 2012
Small-angle scattering and 3D structure interpretation Trewhella, Jill Current Opinion in Structural Biology, Vol. 40 https://doi.org/10.1016/j.sbi.2016.05.003	journal	October 2016
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 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
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010
Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments 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 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
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
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
Glycan reader: Automated sugar identification and simulation preparation for carbohydrates and glycoproteins Jo, Sunhwan; Song, Kevin C.; Desaire, Heather Journal of Computational Chemistry, Vol. 32, Issue 14 https://doi.org/10.1002/jcc.21886	journal	August 2011

Cited By (4)

Neutron scattering in the biological sciences: progress and prospects Ashkar, Rana; Bilheux, Hassina Z.; Bordallo, Heliosa Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 12 https://doi.org/10.1107/s2059798318017503	journal	December 2018
Direct Electron Transfer of Enzymes Facilitated by Cytochromes Ma, Su; Ludwig, Roland ChemElectroChem, Vol. 6, Issue 4 https://doi.org/10.1002/celc.201801256	journal	December 2018
Distinct Substrate Specificities and Electron-Donating Systems of Fungal Lytic Polysaccharide Monooxygenases Frommhagen, Matthias; Westphal, Adrie H.; van Berkel, Willem J. H. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01080	journal	May 2018
Direct Electron Transfer of Enzymes Facilitated by Cytochromes Ma, Su; Ludwig, Roland ChemElectroChem, Vol. 6, Issue 4 https://doi.org/10.1002/celc.201900058	journal	January 2019

Similar Records

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

Journal Article · Wed Jan 31 00:00:00 EST 2018 · Biochimica et Biophysica Acta - General Subjects · OSTI ID:1424447

Bodenheimer, Annette M.; O'Dell, William B.; Oliver, Ryan C.; +3 more

Cellobionic acid utilization: from Neurospora crassa to Saccharomyces cerevisiae

Journal Article · Sun Aug 16 00:00:00 EDT 2015 · Biotechnology for Biofuels · OSTI ID:1424447

Li, Xin; Chomvong, Kulika; Yu, Vivian Yaci; +3 more

Oxygen Activation at the Active Site of a Fungal Lytic Polysaccharide Monooxygenase

Journal Article · Thu Dec 22 00:00:00 EST 2016 · Angewandte Chemie · OSTI ID:1424447

O'Dell, William B.; Agarwal, Pratul K.; Meilleur, Flora

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
polysaccharide monooxygenases
cellobiose dehydrogenases
neutron diffraction
neutron scattering
x-ray induced photoreduction

Title: Structural studies of Neurospora crassa LPMO9D and redox partner CDHIIA using neutron crystallography and small-angle scattering

Citation Formats

References (33)

Cited By (4)

Similar Records

Related Subjects