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Title: Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition

Abstract

Lytic polysaccharide monooxygenases (LPMOs) are a group of recently discovered enzymes that play important roles in the decomposition of recalcitrant polysaccharides. Here, we report the biochemical, structural, and computational characterization of an LPMO from the white-rot fungus Heterobasidion irregulare (HiLPMO9B). This enzyme oxidizes cellulose at the C1 carbon of glycosidic linkages. The crystal structure of HiLPMO9B was determined at 2.1 A resolution using X-ray crystallography. Unlike the majority of the currently available C1-specific LPMO structures, the HiLPMO9B structure contains an extended L2 loop, connecting ..beta..-strands ..beta..2 and ..beta..3 of the ..beta..-sandwich structure. Molecular dynamics (MD) simulations suggest roles for both aromatic and acidic residues in the substrate binding of HiLPMO9B, with the main contribution from the residues located on the extended region of the L2 loop (Tyr20) and the LC loop (Asp205, Tyr207, and Glu210). Asp205 and Glu210 were found to be involved in the hydrogen bonding with the hydroxyl group of the C6 carbon of glucose moieties directly or via a water molecule. Two different binding orientations were observed over the course of the MD simulations. In each orientation, the active-site copper of this LPMO preferentially skewed toward the pyranose C1 of the glycosidic linkage over the targeted glycosidicmore » bond. This study provides additional insight into cellulose binding by C1-specific LPMOs, giving a molecular-level picture of active site substrate interactions.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [4];  [5];  [6];  [1]
  1. Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala Sweden
  2. Department of Chemical and Materials Engineering, University of Kentucky, Lexington KY USA
  3. Department of Chemistry, Biotechnology, and Food Science, Norwegian University of Life Sciences, Ås Norway
  4. Biosciences Center, National Renewable Energy Laboratory, Golden CO USA
  5. Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala Sweden; Department of Chemical Engineering, University of Patras, Greece
  6. Department of Chemical and Materials Engineering, University of Kentucky, Lexington KY USA; Directorate of Engineering, Division of Chemical, Bioengineering, Environmental, and Transport Systems, National Science Foundation, Alexandria VA USA
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office (EE-3B)
OSTI Identifier:
1436073
Report Number(s):
NREL/JA-2700-71451
Journal ID: ISSN 1742-464X
DOE Contract Number:  
AC36-08GO28308
Resource Type:
Journal Article
Journal Name:
Federation of European Biochemical Societies (FEBS) Journal
Additional Journal Information:
Journal Volume: none; Journal Issue: none; Journal ID: ISSN 1742-464X
Publisher:
Federation of European Biochemical Societies
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; AA9; computational simulation; crystal structure; Heterobasidion irregulare; lytic polysaccharide monooxygenase (LPMO); substrate interaction

Citation Formats

Liu, Bing, Kognole, Abhishek A., Wu, Miao, Westereng, Bjørge, Crowley, Michael F., Kim, Seonah, Dimarogona, Maria, Payne, Christina M., and Sandgren, Mats. Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition. United States: N. p., 2018. Web. doi:10.1111/febs.14472.
Liu, Bing, Kognole, Abhishek A., Wu, Miao, Westereng, Bjørge, Crowley, Michael F., Kim, Seonah, Dimarogona, Maria, Payne, Christina M., & Sandgren, Mats. Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition. United States. doi:10.1111/febs.14472.
Liu, Bing, Kognole, Abhishek A., Wu, Miao, Westereng, Bjørge, Crowley, Michael F., Kim, Seonah, Dimarogona, Maria, Payne, Christina M., and Sandgren, Mats. Tue . "Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition". United States. doi:10.1111/febs.14472.
@article{osti_1436073,
title = {Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition},
author = {Liu, Bing and Kognole, Abhishek A. and Wu, Miao and Westereng, Bjørge and Crowley, Michael F. and Kim, Seonah and Dimarogona, Maria and Payne, Christina M. and Sandgren, Mats},
abstractNote = {Lytic polysaccharide monooxygenases (LPMOs) are a group of recently discovered enzymes that play important roles in the decomposition of recalcitrant polysaccharides. Here, we report the biochemical, structural, and computational characterization of an LPMO from the white-rot fungus Heterobasidion irregulare (HiLPMO9B). This enzyme oxidizes cellulose at the C1 carbon of glycosidic linkages. The crystal structure of HiLPMO9B was determined at 2.1 A resolution using X-ray crystallography. Unlike the majority of the currently available C1-specific LPMO structures, the HiLPMO9B structure contains an extended L2 loop, connecting ..beta..-strands ..beta..2 and ..beta..3 of the ..beta..-sandwich structure. Molecular dynamics (MD) simulations suggest roles for both aromatic and acidic residues in the substrate binding of HiLPMO9B, with the main contribution from the residues located on the extended region of the L2 loop (Tyr20) and the LC loop (Asp205, Tyr207, and Glu210). Asp205 and Glu210 were found to be involved in the hydrogen bonding with the hydroxyl group of the C6 carbon of glucose moieties directly or via a water molecule. Two different binding orientations were observed over the course of the MD simulations. In each orientation, the active-site copper of this LPMO preferentially skewed toward the pyranose C1 of the glycosidic linkage over the targeted glycosidic bond. This study provides additional insight into cellulose binding by C1-specific LPMOs, giving a molecular-level picture of active site substrate interactions.},
doi = {10.1111/febs.14472},
journal = {Federation of European Biochemical Societies (FEBS) Journal},
issn = {1742-464X},
number = none,
volume = none,
place = {United States},
year = {2018},
month = {4}
}

Works referenced in this record:

Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases
journal, January 2014

  • Book, Adam J.; Yennamalli, Ragothaman M.; Takasuka, Taichi E.
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/1754-6834-7-109

CHAINSAW : a program for mutating pdb files used as templates in molecular replacement
journal, April 2008


Secretome data from Trichoderma reesei and Aspergillus niger cultivated in submerged and sequential fermentation methods
journal, September 2016


Novel enzymes for the degradation of cellulose
journal, January 2012

  • Horn, Svein; Vaaje-Kolstad, Gustav; Westereng, Bjørge
  • Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 45
  • DOI: 10.1186/1754-6834-5-45

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

Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism
journal, December 2013

  • Kim, S.; Stahlberg, J.; Sandgren, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 1
  • DOI: 10.1073/pnas.1316609111

On the catalytic mechanisms of lytic polysaccharide monooxygenases
journal, April 2016


Fungal Cellulases
journal, January 2015

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

Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997

  • Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
  • DOI: 10.1107/S0907444996012255

The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases
journal, February 2016

  • Frandsen, Kristian E. H.; Simmons, Thomas J.; Dupree, Paul
  • Nature Chemical Biology, Vol. 12, Issue 4
  • DOI: 10.1038/nchembio.2029

Binding Preferences, Surface Attachment, Diffusivity, and Orientation of a Family 1 Carbohydrate-binding Module on Cellulose
journal, April 2012

  • Nimlos, Mark R.; Beckham, Gregg T.; Matthews, James F.
  • Journal of Biological Chemistry, Vol. 287, Issue 24
  • DOI: 10.1074/jbc.M112.358184

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Efficient separation of oxidized cello-oligosaccharides generated by cellulose degrading lytic polysaccharide monooxygenases
journal, January 2013


Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family
journal, April 2010

  • Harris, Paul; Welner, Ditte; McFarland, K.
  • Biochemistry, Vol. 49, Issue 15, p. 3305-3316
  • DOI: 10.1021/bi100009p

Crystal Structure and Computational Characterization of the Lytic Polysaccharide Monooxygenase GH61D from the Basidiomycota Fungus Phanerochaete chrysosporium
journal, March 2013

  • Wu, Miao; Beckham, Gregg T.; Larsson, Anna M.
  • Journal of Biological Chemistry, Vol. 288, Issue 18
  • DOI: 10.1074/jbc.M113.459396

Molecular-Level Origins of Biomass Recalcitrance: Decrystallization Free Energies for Four Common Cellulose Polymorphs
journal, April 2011

  • Beckham, Gregg T.; Matthews, James F.; Peters, Baron
  • The Journal of Physical Chemistry B, Vol. 115, Issue 14
  • DOI: 10.1021/jp1106394

An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides
journal, October 2010

  • Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J.
  • Science, Vol. 330, Issue 6001, p. 219-222
  • DOI: 10.1126/science.1192231

A Structural Overview of gh61 Proteins – Fungal Cellulose Degrading Polysaccharide Monooxygenases
journal, September 2012

  • Leggio, Leila Lo; Welner, Ditte; De Maria, Leonardo
  • Computational and Structural Biotechnology Journal, Vol. 2, Issue 3
  • DOI: 10.5936/csbj.201209019

Distribution and diversity of enzymes for polysaccharide degradation in fungi
journal, March 2017


Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components
journal, August 2011

  • Quinlan, R. J.; Sweeney, M. D.; Lo Leggio, L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 37, p. 15079-15084
  • DOI: 10.1073/pnas.1105776108

Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

Lytic polysaccharide monooxygenases disrupt the cellulose fibers structure
journal, January 2017

  • Villares, Ana; Moreau, Céline; Bennati-Granier, Chloé
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep40262

Simultaneous analysis of C1 and C4 oxidized oligosaccharides, the products of lytic polysaccharide monooxygenases acting on cellulose
journal, May 2016


A C4-oxidizing Lytic Polysaccharide Monooxygenase Cleaving Both Cellulose and Cello-oligosaccharides
journal, December 2013

  • Isaksen, Trine; Westereng, Bjørge; Aachmann, Finn L.
  • Journal of Biological Chemistry, Vol. 289, Issue 5
  • DOI: 10.1074/jbc.M113.530196

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

Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2
journal, August 2017

  • Bissaro, Bastien; Røhr, Åsmund K.; Müller, Gerdt
  • Nature Chemical Biology, Vol. 13, Issue 10
  • DOI: 10.1038/nchembio.2470

The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans
journal, March 2017

  • Fanuel, Mathieu; Garajova, Sona; Ropartz, David
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0749-5

Transcriptome and Secretome Analyses of Phanerochaete chrysosporium Reveal Complex Patterns of Gene Expression
journal, April 2009

  • Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M.
  • Applied and Environmental Microbiology, Vol. 75, Issue 12
  • DOI: 10.1128/AEM.00314-09

All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins
journal, April 1998

  • MacKerell, A. D.; Bashford, D.; Bellott, M.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 18
  • DOI: 10.1021/jp973084f

Additive empirical force field for hexopyranose monosaccharides
journal, November 2008

  • Guvench, Olgun; Greene, Shannon N.; Kamath, Ganesh
  • Journal of Computational Chemistry, Vol. 29, Issue 15
  • DOI: 10.1002/jcc.21004

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

Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation
journal, April 2014

  • Agger, J. W.; Isaksen, T.; Varnai, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1323629111

Cellulose Surface Degradation by a Lytic Polysaccharide Monooxygenase and Its Effect on Cellulase Hydrolytic Efficiency
journal, October 2014

  • Eibinger, Manuel; Ganner, Thomas; Bubner, Patricia
  • Journal of Biological Chemistry, Vol. 289, Issue 52
  • DOI: 10.1074/jbc.M114.602227

CHARMM: The biomolecular simulation program
journal, July 2009

  • Brooks, B. R.; Brooks, C. L.; Mackerell, A. D.
  • Journal of Computational Chemistry, Vol. 30, Issue 10
  • DOI: 10.1002/jcc.21287

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


XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Solvent-Induced Forces between Two Hydrophilic Groups
journal, February 1994

  • Durell, Stewart R.; Brooks, Bernard R.; Ben-Naim, Arieh
  • The Journal of Physical Chemistry, Vol. 98, Issue 8
  • DOI: 10.1021/j100059a038

Lytic polysaccharide monooxygenases: a crystallographer's view on a new class of biomass-degrading enzymes
journal, October 2016


The Role of the Secondary Coordination Sphere in a Fungal Polysaccharide Monooxygenase
journal, March 2017


Oxidative Cleavage of Cellulose by Fungal Copper-Dependent Polysaccharide Monooxygenases
journal, December 2011

  • Beeson, William T.; Phillips, Christopher M.; Cate, Jamie H. D.
  • Journal of the American Chemical Society, Vol. 134, Issue 2
  • DOI: 10.1021/ja210657t

Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina
journal, June 2015

  • Bennati-Granier, Chloé; Garajova, Sona; Champion, Charlotte
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0274-3

ExPASy: the proteomics server for in-depth protein knowledge and analysis
journal, July 2003


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

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 Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose
journal, November 2011


Fungal cellulose degradation by oxidative enzymes: from dysfunctional GH61 family to powerful lytic polysaccharide monooxygenase family
journal, September 2014

  • Morgenstern, I.; Powlowski, J.; Tsang, A.
  • Briefings in Functional Genomics, Vol. 13, Issue 6
  • DOI: 10.1093/bfgp/elu032

Lytic Polysaccharide Monooxygenases: The Microbial Power Tool for Lignocellulose Degradation
journal, November 2016


MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Deciphering key features in protein structures with the new ENDscript server
journal, April 2014

  • Robert, Xavier; Gouet, Patrice
  • Nucleic Acids Research, Vol. 42, Issue W1
  • DOI: 10.1093/nar/gku316

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61
journal, August 2011

  • Langston, James A.; Shaghasi, Tarana; Abbate, Eric
  • Applied and Environmental Microbiology, Vol. 77, Issue 19, p. 7007-7015
  • DOI: 10.1128/AEM.05815-11

Carbohydrate-binding modules: fine-tuning polysaccharide recognition
journal, September 2004

  • Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J.
  • Biochemical Journal, Vol. 382, Issue 3
  • DOI: 10.1042/BJ20040892

Fg LPMO9A from Fusarium graminearum cleaves xyloglucan independently of the backbone substitution pattern
journal, September 2016

  • Nekiunaite, Laura; Petrović, Dejan M.; Westereng, Bjørge
  • FEBS Letters, Vol. 590, Issue 19
  • DOI: 10.1002/1873-3468.12385

Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase
journal, January 2015

  • Lo Leggio, Leila; Simmons, Thomas J.; Poulsen, Jens-Christian N.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms6961

Structural and Functional Characterization of a Lytic Polysaccharide Monooxygenase with Broad Substrate Specificity
journal, July 2015

  • Borisova, Anna S.; Isaksen, Trine; Dimarogona, Maria
  • Journal of Biological Chemistry, Vol. 290, Issue 38
  • DOI: 10.1074/jbc.M115.660183

Lytic Polysaccharide Monooxygenases in Biomass Conversion
journal, December 2015


Using a model filamentous fungus to unravel mechanisms of lignocellulose deconstruction
journal, January 2013

  • Znameroski, Elizabeth A.; Glass, N. Louise
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-6

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

An introduction to data reduction: space-group determination, scaling and intensity statistics
journal, March 2011

  • Evans, Philip R.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S090744491003982X

CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses
journal, August 2009

  • Guvench, Olgun; Hatcher, Elizabeth; Venable, Richard M.
  • Journal of Chemical Theory and Computation, Vol. 5, Issue 9
  • DOI: 10.1021/ct900242e

Type-dependent action modes of TtAA9E and TaAA9A acting on cellulose and differently pretreated lignocellulosic substrates
journal, February 2017


Phi/Psi-chology: Ramachandran revisited
journal, December 1996


Free R value: a novel statistical quantity for assessing the accuracy of crystal structures
journal, January 1992


CHARMM Additive All-Atom Force Field for Carbohydrate Derivatives and Its Utility in Polysaccharide and Carbohydrate–Protein Modeling
journal, August 2011

  • Guvench, Olgun; Mallajosyula, Sairam S.; Raman, E. Prabhu
  • Journal of Chemical Theory and Computation, Vol. 7, Issue 10
  • DOI: 10.1021/ct200328p

The First Structure of a Glycoside Hydrolase Family 61 Member, Cel61B from Hypocrea jecorina, at 1.6 Å Resolution
journal, October 2008

  • Karkehabadi, Saeid; Hansson, Henrik; Kim, Steve
  • Journal of Molecular Biology, Vol. 383, Issue 1, p. 144-154
  • DOI: 10.1016/j.jmb.2008.08.016

Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates
journal, October 2017


Determinants of Regioselective Hydroxylation in the Fungal Polysaccharide Monooxygenases
journal, December 2013

  • Vu, Van V.; Beeson, William T.; Phillips, Christopher M.
  • Journal of the American Chemical Society, Vol. 136, Issue 2
  • DOI: 10.1021/ja409384b

Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction
journal, August 2002

  • Nishiyama, Yoshiharu; Langan, Paul; Chanzy, Henri
  • Journal of the American Chemical Society, Vol. 124, Issue 31
  • DOI: 10.1021/ja0257319

Classification of fungal and bacterial lytic polysaccharide monooxygenases
journal, May 2015


Cellulose Degradation by Polysaccharide Monooxygenases
journal, June 2015


Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206