Structural Basis of Stereospecificity in the Bacterial Enzymatic Cleavage of β-Aryl Ether Bonds in Lignin

Helmich, Kate E.; Pereira, Jose Henrique; Gall, Daniel L.; Heins, Richard A.; McAndrew, Ryan P.; Bingman, Craig; Deng, Kai; Holland, Keefe C.; Noguera, Daniel R.; Simmons, Blake A.; Sale, Kenneth L.; Ralph, John; Donohue, Timothy J.; Adams, Paul D.; Phillips, Jr., George N.

doi:10.1074/jbc.M115.694307

Title: Structural Basis of Stereospecificity in the Bacterial Enzymatic Cleavage of β-Aryl Ether Bonds in Lignin

Journal Article · Mon Feb 29 23:00:00 EST 2016 · Journal of Biological Chemistry

DOI: https://doi.org/10.1074/jbc.M115.694307 · OSTI ID:1782304

Helmich, Kate E.; Pereira, Jose Henrique; Gall, Daniel L.; Heins, Richard A.; McAndrew, Ryan P.; Bingman, Craig; Deng, Kai; Holland, Keefe C.; Noguera, Daniel R.; Simmons, Blake A.; Sale, Kenneth L.; Ralph, John; Donohue, Timothy J.; Adams, Paul D.; Phillips, Jr., George N.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357; FC02-07ER64494

OSTI ID:: 1782304

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 10 Vol. 291; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Sequence complexity of disordered protein Romero, Pedro; Obradovic, Zoran; Li, Xiaohong Proteins: Structure, Function, and Genetics, Vol. 42, Issue 1 https://doi.org/10.1002/1097-0134(20010101)42:1<38::AID-PROT50>3.0.CO;2-3	journal	January 2000
Fungal laccase: properties and activity on lignin Leonowicz, Andrzej; Cho, NamSeok; Luterek, Jolanta Journal of Basic Microbiology, Vol. 41, Issue 3-4 https://doi.org/10.1002/1521-4028(200107)41:3/4<185::AID-JOBM185>3.0.CO;2-T	journal	July 2001
Specification of Molecular Chirality Cahn, R. S.; Ingold, Christopher; Prelog, V. Angewandte Chemie International Edition in English, Vol. 5, Issue 4 https://doi.org/10.1002/anie.196603851	journal	April 1966
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
Fast docking using the CHARMM force field with EADock DSS Grosdidier, Aurélien; Zoete, Vincent; Michielin, Olivier Journal of Computational Chemistry, Vol. 32, Issue 10 https://doi.org/10.1002/jcc.21797	journal	May 2011
Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts Klock, Heath E.; Koesema, Eric J.; Knuth, Mark W. Proteins: Structure, Function, and Bioinformatics, Vol. 71, Issue 2 https://doi.org/10.1002/prot.21786	journal	January 2008
Structure Determination and Refinement of Human Alpha Class Glutathione Transferase A1-1, and a Comparison with the Mu and Pi Class Enzymes Sinning, Irmgard; Kleywegt, Gerard J.; Cowan, Sandra W. Journal of Molecular Biology, Vol. 232, Issue 1 https://doi.org/10.1006/jmbi.1993.1376	journal	July 1993
Refined Crystal Structure of Porcine Class Pi Glutathione S-Transferase (pGST P1-1) at 2·1 Å Resolution Dirr, Heini; Reinemer, Peter; Huber, Robert Journal of Molecular Biology, Vol. 243, Issue 1 https://doi.org/10.1006/jmbi.1994.1631	journal	October 1994
Three-dimensional structure of Escherichia coli glutathione S-transferase complexed with glutathione sulfonate: catalytic roles of Cys10 and His106 Nishida, Motohiko; Harada, Shigeharu; Noguchi, Shuji Journal of Molecular Biology, Vol. 281, Issue 1 https://doi.org/10.1006/jmbi.1998.1927	journal	August 1998
Proof of the presence of racemic forms of arylglycerol-Β-aryl ether structure in lignin: studies on the stereo structure of lignin by ozonation Akiyama, Takuya; Magara, Kengo; Matsumoto, Yuji Journal of Wood Science, Vol. 46, Issue 5 https://doi.org/10.1007/BF00776407	journal	October 2000
Site-directed mutagenesis of the Proteus mirabilis glutathione transferase B1-1 G-site Casalone, Enrico; Allocati, Nerino; Ceccarelli, Ilaria FEBS Letters, Vol. 423, Issue 2 https://doi.org/10.1016/S0014-5793(98)00080-5	journal	February 1998
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Human theta class glutathione transferase: the crystal structure reveals a sulfate-binding pocket within a buried active site Rossjohn, Jamie; McKinstry, William J.; Oakley, Aaron J. Structure, Vol. 6, Issue 3 https://doi.org/10.1016/S0969-2126(98)00034-3	journal	March 1998
A mixed disulfide bond in bacterial glutathione transferase: functional and evolutionary implications Rossjohn, Jamie; Polekhina, Galina; Feil, Susanne C. Structure, Vol. 6, Issue 6 https://doi.org/10.1016/S0969-2126(98)00074-4	journal	June 1998
The emerging role for bacteria in lignin degradation and bio-product formation Bugg, Timothy DH; Ahmad, Mark; Hardiman, Elizabeth M. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2010.10.009	journal	June 2011
Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class Meux, Edgar; Prosper, Pascalita; Masai, Eiji FEBS Letters, Vol. 586, Issue 22 https://doi.org/10.1016/j.febslet.2012.09.036	journal	October 2012
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium Sreenath, Hassan K.; Bingman, Craig A.; Buchan, Blake W. Protein Expression and Purification, Vol. 40, Issue 2 https://doi.org/10.1016/j.pep.2004.12.022	journal	April 2005
Three-dimensional structure, catalytic properties, and evolution of a sigma class glutathione transferase from squid, a progenitor of the lens S-crystallins of cephalopods Ji, Xinhua; von Rosenvinge, Erik C.; Johnson, William W. Biochemistry, Vol. 34, Issue 16 https://doi.org/10.1021/bi00016a003	journal	April 1995
Structure and Function of the Xenobiotic Substrate Binding Site of a Glutathione S-Transferase as Revealed by X-ray Crystallographic Analysis of Product Complexes with the Diastereomers of 9-(S-Glutathionyl)-10-hydroxy-9,10-dihydrophenanthrene Ji, Xinhua; Johnson, William W.; Sesay, Muctarr A. Biochemistry, Vol. 33, Issue 5 https://doi.org/10.1021/bi00171a002	journal	February 1994
ChemDraw Ultra 10.0 CambridgeSoft, 100 CambridgePark Drive, Cambridge, MA 02140. www.cambridgesoft.com. Commercial Price: $1910 for download, $2150 for CD-ROM; Academic Price: $710 for download, $800 for CD-ROM. Mills, Nancy Journal of the American Chemical Society, Vol. 128, Issue 41 https://doi.org/10.1021/ja0697875	journal	October 2006
Are Lignins Optically Active? Ralph, John; Peng, Junpeng; Lu, Fachuang Journal of Agricultural and Food Chemistry, Vol. 47, Issue 8 https://doi.org/10.1021/jf9901136	journal	August 1999
Structure, Catalytic Mechanism, and Evolution of the Glutathione Transferases Armstrong, Richard N. Chemical Research in Toxicology, Vol. 10, Issue 1 https://doi.org/10.1021/tx960072x	journal	January 1997
Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids Ralph, John; Lundquist, Knut; Brunow, Gösta Phytochemistry Reviews, Vol. 3, Issue 1-2, p. 29-60 https://doi.org/10.1023/B:PHYT.0000047809.65444.a4	journal	January 2004
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Exploring glutathione lyases as biocatalysts: paving the way for enzymatic lignin depolymerization and future stereoselective applications Picart, Pere; Sevenich, Marc; Domínguez de María, Pablo Green Chem., Vol. 17, Issue 11 https://doi.org/10.1039/C5GC01078K	journal	January 2015
Pathways for degradation of lignin in bacteria and fungi Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M. Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896 https://doi.org/10.1039/c1np00042j	journal	January 2011
Enzymatic cleavage of lignin β-O-4 aryl ether bonds via net internal hydrogen transfer Reiter, Jochen; Strittmatter, Harald; Wiemann, Lars O. Green Chemistry, Vol. 15, Issue 5 https://doi.org/10.1039/c3gc40295a	journal	January 2013
Role of Ser11 in the stabilization of the structure of Ochrobactrum anthropi glutathione transferase Federici, Luca; Masulli, Michele; Bonivento, Daniele Biochemical Journal, Vol. 403, Issue 2 https://doi.org/10.1042/BJ20061707	journal	March 2007
Novel class of glutathione transferases from cyanobacteria exhibit high catalytic activities towards naturally occurring isothiocyanates Wiktelius, Eric; Stenberg, Gun Biochemical Journal, Vol. 406, Issue 1 https://doi.org/10.1042/BJ20070328	journal	July 2007
Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily Sheehan, David; Meade, Gerardene; Foley, Vivienne M. Biochemical Journal, Vol. 360, Issue 1 https://doi.org/10.1042/bj3600001	journal	November 2001
Novel Folding and Stability Defects Cause a Deficiency of Human Glutathione Transferase Omega 1 Zhou, Huina; Brock, Joseph; Casarotto, Marco G. Journal of Biological Chemistry, Vol. 286, Issue 6 https://doi.org/10.1074/jbc.M110.197822	journal	November 2010
Characterization of a Phanerochaete chrysosporium Glutathione Transferase Reveals a Novel Structural and Functional Class with Ligandin Properties Mathieu, Yann; Prosper, Pascalita; Buée, Marc Journal of Biological Chemistry, Vol. 287, Issue 46 https://doi.org/10.1074/jbc.M112.402776	journal	September 2012
Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway Gall, Daniel L.; Kim, Hoon; Lu, Fachuang Journal of Biological Chemistry, Vol. 289, Issue 12 https://doi.org/10.1074/jbc.M113.536250	journal	February 2014
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
SwissDock, a protein-small molecule docking web service based on EADock DSS Grosdidier, A.; Zoete, V.; Michielin, O. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr366	journal	May 2011
Automated matching of high- and low-resolution structural models Kozin, M. B.; Svergun, D. I. Journal of Applied Crystallography, Vol. 34, Issue 1, p. 33-41 https://doi.org/10.1107/S0021889800014126	journal	February 2001
Uniqueness of ab initio shape determination in small-angle scattering Volkov, Vladimir V.; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864 https://doi.org/10.1107/S0021889803000268	journal	April 2003
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
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
Automatic multiple-zone rigid-body refinement with a large convergence radius Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Urzhumtsev, Alexandre Journal of Applied Crystallography, Vol. 42, Issue 4 https://doi.org/10.1107/S0021889809023528	journal	July 2009
Sparse matrix sampling: a screening method for crystallization of proteins Jancarik, J.; Kim, S. H. Journal of Applied Crystallography, Vol. 24, Issue 4 https://doi.org/10.1107/S0021889891004430	journal	August 1991
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
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S090744490705024X	journal	December 2007
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909012098	journal	May 2009
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
Using a commodity high-definition television for collaborative structural biology Yennamalli, Ragothaman; Arangarasan, Raj; Bryden, Aaron Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S160057671400939X	journal	May 2014
X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function Dirr, Heini; Reinemer, Peter; Huber, Robert European Journal of Biochemistry, Vol. 220, Issue 3 https://doi.org/10.1111/j.1432-1033.1994.tb18666.x	journal	March 1994
Glutathione transferases in bacteria: Bacterial GSTs Allocati, Nerino; Federici, Luca; Masulli, Michele FEBS Journal, Vol. 276, Issue 1 https://doi.org/10.1111/j.1742-4658.2008.06743.x	journal	November 2008
Lignin Valorization: Improving Lignin Processing in the Biorefinery Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J. Science, Vol. 344, Issue 6185, p. 1246843-1246843 https://doi.org/10.1126/science.1246843	journal	May 2014
Determination of macromolecular structures from anomalous diffraction of synchrotron radiation Hendrickson, W. Science, Vol. 254, Issue 5028 https://doi.org/10.1126/science.1925561	journal	October 1991
Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6 Sato, Y.; Moriuchi, H.; Hishiyama, S. Applied and Environmental Microbiology, Vol. 75, Issue 16 https://doi.org/10.1128/AEM.00880-09	journal	June 2009
Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether Masai, E.; Ichimura, A.; Sato, Y. Journal of Bacteriology, Vol. 185, Issue 6 https://doi.org/10.1128/JB.185.6.1768-1775.2003	journal	March 2003
Glutathione Transferases Hayes, John D.; Flanagan, Jack U.; Jowsey, Ian R. Annual Review of Pharmacology and Toxicology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.pharmtox.45.120403.095857	journal	September 2005
Open Babel: An open chemical toolbox O'Boyle, Noel M.; Banck, Michael; James, Craig A. Journal of Cheminformatics, Vol. 3, Issue 1 https://doi.org/10.1186/1758-2946-3-33	journal	October 2011
Next-generation biomass feedstocks for biofuel production Simmons, Blake A.; Loque, Dominique; Blanch, Harvey W. Genome Biology, Vol. 9, Issue 12 https://doi.org/10.1186/gb-2008-9-12-242	journal	January 2008
Metatranscriptomic analysis of lignocellulolytic microbial communities involved in high-solids decomposition of rice straw Simmons, Christopher W.; Reddy, Amitha P.; D’haeseleer, Patrik Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0180-0	journal	December 2014
Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds Masai, Eiji; Katayama, Yoshihiro; Fukuda, Masao Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1271/bbb.60437	journal	January 2007
Simplified, Enhanced Protein Purification Using an Inducible, Autoprocessing Enzyme Tag Shen, Aimee; Lupardus, Patrick J.; Morell, Montse PLoS ONE, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pone.0008119	journal	December 2009
Discovery of Microorganisms and Enzymes Involved in High-Solids Decomposition of Rice Straw Using Metagenomic Analyses Reddy, Amitha P.; Simmons, Christopher W.; D’haeseleer, Patrik PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0077985	journal	October 2013
Diversification of Fungal Specific Class A Glutathione Transferases in Saprotrophic Fungi Mathieu, Yann; Prosper, Pascalita; Favier, Frédérique PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0080298	journal	November 2013
The Erythro/Threo Ratio of β-O-4 Structures as an Important Structural Characteristic of Lignin. Part 2. Changes in Erythro/Threo (E/T) Ratio of β-O-4 Structures during Delignification Reactions Sugimoto, T.; Akiyama, T.; Matsumoto, Y. Holzforschung, Vol. 56, Issue 4 https://doi.org/10.1515/HF.2002.064	journal	June 2002
Glutathione transferases: a structural perspective Oakley, Aaron Drug Metabolism Reviews, Vol. 43, Issue 2 https://doi.org/10.3109/03602532.2011.558093	journal	March 2011
Functional Diversification of Fungal Glutathione Transferases from the Ure2p Class Thuillier, Anne; Ngadin, Andrew A.; Thion, Cécile International Journal of Evolutionary Biology, Vol. 2011 https://doi.org/10.4061/2011/938308	journal	January 2011

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