Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

Book, Adam J.; Yennamalli, Ragothaman M.; Takasuka, Taichi E.; Currie, Cameron R.; Phillips, George N.; Fox, Brian G.

doi:10.1186/1754-6834-7-109

Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

Journal Article · Wed Aug 06 00:00:00 EDT 2014 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/1754-6834-7-109· OSTI ID:1626659

Book, Adam J. ^[1]; Yennamalli, Ragothaman M. ^[2]; Takasuka, Taichi E. ^[3]; Currie, Cameron R. ^[4]; Phillips, George N. ^[5]; Fox, Brian G. ^[3]

Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology; DOE/OSTI
Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Biochemistry Addition
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Biochemistry Addition

Background: Understanding the diversity of lignocellulose-degrading enzymes in nature will provide insights for the improvement of cellulolytic enzyme cocktails used in the biofuels industry. Two families of enzymes, fungal AA9 and bacterial AA10, have recently been characterized as crystalline cellulose or chitin-cleaving lytic polysaccharide monooxygenases (LPMOs). Here we analyze the sequences, structures, and evolution of LPMOs to understand the factors that may influence substrate specificity both within and between these enzyme families. Results: Comparative analysis of sequences, solved structures, and homology models from AA9 and AA10 LPMO families demonstrated that, although these two LPMO families are highly conserved, structurally they have minimal sequence similarity outside the active site residues. Phylogenetic analysis of the AA10 family identified clades with putative chitinolytic and cellulolytic activities. Estimation of the rate of synonymous versus non-synonymous substitutions (dN/dS) within two major AA10 subclades showed distinct selective pressures between putative cellulolytic genes (subclade A) and CBP21-like chitinolytic genes (subclade D). Estimation of site-specific selection demonstrated that changes in the active sites were strongly negatively selected in all subclades. Furthermore, all codons in the subclade D had dN/dS values of less than 0.7, whereas codons in the cellulolytic subclade had dN/dS values of greater than 1.5. Positively selected codons were enriched at sites localized on the surface of the protein adjacent to the active site. Conclusions: The structural similarity but absence of significant sequence similarity between AA9 and AA10 families suggests that these enzyme families share an ancient ancestral protein. Combined analysis of amino acid sites under Darwinian selection and structural homology modeling identified a subclade of AA10 with diversifying selection at different surfaces, potentially used for cellulose-binding and protein-protein interactions. Together, these data indicate that AA10 LPMOs are under selection to change their function, which may optimize cellulolytic activity. This work provides a phylogenetic basis for identifying and classifying additional cellulolytic or chitinolytic LPMOs.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FC02-07ER64494; FG02-04ER25627

OSTI ID:: 1626659

Journal Information:: Biotechnology for Biofuels, Journal Name: Biotechnology for Biofuels Journal Issue: 1 Vol. 7; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Gene cloning and characterization of a novel α-amylase from alkaliphilicAlkalimonas amylolytica Wang, Nan; Zhang, Yunhua; Wang, Quanhui Biotechnology Journal, Vol. 1, Issue 11 https://doi.org/10.1002/biot.200600098	journal	November 2006
Regulation and characterization of Thermobifida fusca carbohydrate-binding module proteins E7 and E8 Moser, Felix; Irwin, Diana; Chen, Shaolin Biotechnology and Bioengineering, Vol. 100, Issue 6, p. 1066-1077 https://doi.org/10.1002/bit.21856	journal	January 2008
Cleavage of cellulose by a CBM33 protein Forsberg, Zarah; Vaaje-Kolstad, Gustav; Westereng, Bjørge Protein Science, Vol. 20, Issue 9 https://doi.org/10.1002/pro.689	journal	August 2011
Isolation of genes coding for chitin-degrading enzymes in the novel chitinolytic bacterium, Chitiniphilus shinanonensis, and characterization of a gene coding for a family 19 chitinase Huang, Lanxiang; Garbulewska, Ewelina; Sato, Kazuaki Journal of Bioscience and Bioengineering, Vol. 113, Issue 3 https://doi.org/10.1016/j.jbiosc.2011.10.018	journal	March 2012
The First Structure of a Glycoside Hydrolase Family 61 Member, Cel61B from Hypocrea jecorina, at 1.6 Å Resolution Karkehabadi, Saeid; Hansson, Henrik; Kim, Steve Journal of Molecular Biology, Vol. 383, Issue 1, p. 144-154 https://doi.org/10.1016/j.jmb.2008.08.016	journal	October 2008
Characterization of the Chitinolytic Machinery of Enterococcus faecalis V583 and High-Resolution Structure of Its Oxidative CBM33 Enzyme Vaaje-Kolstad, Gustav; Bøhle, Liv Anette; Gåseidnes, Sigrid Journal of Molecular Biology, Vol. 416, Issue 2 https://doi.org/10.1016/j.jmb.2011.12.033	journal	February 2012
Structural Basis for Substrate Targeting and Catalysis by Fungal Polysaccharide Monooxygenases Li, Xin; Beeson, William T.; Phillips, Christopher M. Structure, Vol. 20, Issue 6, p. 1051-1061 https://doi.org/10.1016/j.str.2012.04.002	journal	June 2012
The Ka/Ks ratio: diagnosing the form of sequence evolution Hurst, Laurence D. Trends in Genetics, Vol. 18, Issue 9 https://doi.org/10.1016/s0168-9525(02)02722-1	journal	September 2002
Characterization of a Thermomonospora fusca exocellulase Zhang, Sheng; Lao, Guifang; Wilson, David B. Biochemistry, Vol. 34, Issue 10 https://doi.org/10.1021/bi00010a030	journal	March 1995
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
Comparative Study of Two Chitin-Active and Two Cellulose-Active AA10-Type Lytic Polysaccharide Monooxygenases Forsberg, Zarah; Røhr, Åsmund Kjendseth; Mekasha, Sophanit Biochemistry, Vol. 53, Issue 10 https://doi.org/10.1021/bi5000433	journal	March 2014
Cellobiose Dehydrogenase and a Copper-Dependent Polysaccharide Monooxygenase Potentiate Cellulose Degradation by Neurospora crassa Phillips, Christopher M.; Beeson, William T.; Cate, Jamie H. ACS Chemical Biology, Vol. 6, Issue 12, p. 1399-1406 https://doi.org/10.1021/cb200351y	journal	December 2011
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
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
Determinants of Regioselective Hydroxylation in the Fungal Polysaccharide Monooxygenases Vu, Van V.; Beeson, William T.; Phillips, Christopher M. Journal of the American Chemical Society, Vol. 136, Issue 2 https://doi.org/10.1021/ja409384b	journal	December 2013
Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants Julca, Irene; Ferrari, Camilla; Flores-Tornero, María Nature Plants, Vol. 7, Issue 8 https://doi.org/10.1038/s41477-021-00958-2	journal	July 2021
Mating pair stabilization mediates bacterial conjugation species specificity Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C. Nature Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/s41564-022-01146-4	journal	June 2022
Continuous evolution of base editors with expanded target compatibility and improved activity Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M. Nature Biotechnology, Vol. 37, Issue 9 https://doi.org/10.1038/s41587-019-0193-0	journal	July 2019
Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces Takasuka, Taichi E.; Book, Adam J.; Lewin, Gina R. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01030	journal	January 2013
The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation Hogg, Deborah; Pell, Gavin; Dupree, Paul Biochemical Journal, Vol. 371, Issue 3 https://doi.org/10.1042/bj20021860	journal	May 2003
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
NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions Aachmann, F. L.; Sorlie, M.; Skjak-Braek, G. Proceedings of the National Academy of Sciences, Vol. 109, Issue 46 https://doi.org/10.1073/pnas.1208822109	journal	October 2012
Crystal Structure and Computational Characterization of the Lytic Polysaccharide Monooxygenase GH61D from the Basidiomycota Fungus Phanerochaete chrysosporium Wu, Miao; Beckham, Gregg T.; Larsson, Anna M. Journal of Biological Chemistry, Vol. 288, Issue 18 https://doi.org/10.1074/jbc.m113.459396	journal	March 2013
Fusion of Dioxygenase and Lignin-binding Domains in a Novel Secreted Enzyme from Cellulolytic Streptomyces sp. SirexAA-E Bianchetti, Christopher M.; Harmann, Connor H.; Takasuka, Taichi E. Journal of Biological Chemistry, Vol. 288, Issue 25 https://doi.org/10.1074/jbc.m113.475848	journal	May 2013
A C4-oxidizing Lytic Polysaccharide Monooxygenase Cleaving Both Cellulose and Cello-oligosaccharides Isaksen, Trine; Westereng, Bjørge; Aachmann, Finn L. Journal of Biological Chemistry, Vol. 289, Issue 5 https://doi.org/10.1074/jbc.m113.530196	journal	December 2013
Crystal Structure and Binding Properties of the Serratia marcescens Chitin-binding Protein CBP21 Vaaje-Kolstad, G.; Houston, D. R.; Riemen, A. H. K. Journal of Biological Chemistry, Vol. 280, Issue 12 https://doi.org/10.1074/jbc.m407175200	journal	December 2004
Understanding the Biological Rationale for the Diversity of Cellulose-directed Carbohydrate-binding Modules in Prokaryotic Enzymes Blake, Anthony W.; McCartney, Lesley; Flint, James E. Journal of Biological Chemistry, Vol. 281, Issue 39 https://doi.org/10.1074/jbc.m605903200	journal	July 2006
PAML: a program package for phylogenetic analysis by maximum likelihood Yang, Ziheng Bioinformatics, Vol. 13, Issue 5 https://doi.org/10.1093/bioinformatics/13.5.555	journal	January 1997
MEME: discovering and analyzing DNA and protein sequence motifs Bailey, T. L.; Williams, N.; Misleh, C. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl198	journal	July 2006
Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method Yang, Z.; Rannala, B. Molecular Biology and Evolution, Vol. 14, Issue 7 https://doi.org/10.1093/oxfordjournals.molbev.a025811	journal	July 1997
Protein structure alignment by incremental combinatorial extension (CE) of the optimal path Shindyalov, I. N.; Bourne, P. E. Protein Engineering Design and Selection, Vol. 11, Issue 9 https://doi.org/10.1093/protein/11.9.739	journal	September 1998
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul Systematic Biology, Vol. 61, Issue 3 https://doi.org/10.1093/sysbio/sys029	journal	February 2012
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
Cello-Oligosaccharide Oxidation Reveals Differences between Two Lytic Polysaccharide Monooxygenases (Family GH61) from Podospora anserina Bey, Mathieu; Zhou, Simeng; Poidevin, Laetitia Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/aem.02942-12	journal	November 2012
Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61 Langston, James A.; Shaghasi, Tarana; Abbate, Eric Applied and Environmental Microbiology, Vol. 77, Issue 19, p. 7007-7015 https://doi.org/10.1128/aem.05815-11	journal	August 2011
Identification of a celE-binding protein and its potential role in induction of the celE gene in Thermomonospora fusca. Lin, E. S.; Wilson, D. B. Journal of Bacteriology, Vol. 170, Issue 9 https://doi.org/10.1128/jb.170.9.3843-3846.1988	journal	January 1988
Production of four Neurospora crassa lytic polysaccharide monooxygenases in Pichia pastoris monitored by a fluorimetric assay Kittl, Roman; Kracher, Daniel; Burgstaller, Daniel Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-79	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
Chitin Binding Protein (CBP21) in the Culture Supernatant of Serratia marcescens 2170 Suzuki, Kazushi; Suzuki, Megumi; Taiyoji, Mayumi Bioscience, Biotechnology, and Biochemistry, Vol. 62, Issue 1 https://doi.org/10.1271/bbb.62.128	journal	January 1998
The Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose Westereng, Bjørge; Ishida, Takuya; Vaaje-Kolstad, Gustav PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027807	journal	November 2011
Accounting For Alignment Uncertainty in Phylogenomics Wu, Martin; Chatterji, Sourav; Eisen, Jonathan A. PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0030288	journal	January 2012
The Vibrio cholerae Colonization Factor GbpA Possesses a Modular Structure that Governs Binding to Different Host Surfaces Wong, Edmond; Vaaje-Kolstad, Gustav; Ghosh, Avishek PLoS Pathogens, Vol. 8, Issue 1 https://doi.org/10.1371/journal.ppat.1002373	journal	January 2012
Architecture and active site of particulate methane monooxygenase Culpepper, Megen A.; Rosenzweig, Amy C. Critical Reviews in Biochemistry and Molecular Biology, Vol. 47, Issue 6 https://doi.org/10.3109/10409238.2012.697865	journal	June 2012
Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay Hori, Chiaki; Gaskell, Jill; Igarashi, Kiyohiko Mycologia, Vol. 105, Issue 6 https://doi.org/10.3852/13-072	journal	November 2013
Computational studies of polyurethanases from Pseudomonas do Canto, Vanessa Petry; Thompson, Claudia Elizabeth; Netz, Paulo Augusto Journal of Molecular Modeling, Vol. 27, Issue 2 https://doi.org/10.1007/s00894-021-04671-x	journal	January 2021
The Ka/Ks ratio: diagnosing the form of sequence evolution Hurst, Laurence D. Trends in Genetics, Vol. 18, Issue 9 https://doi.org/10.1016/S0168-9525(02)02722-1	journal	September 2002
Bio-energy in Europe: changing technology choices Faaij, André P. C. Energy Policy, Vol. 34, Issue 3 https://doi.org/10.1016/j.enpol.2004.03.026	journal	February 2006
Microbial diversity of cellulose hydrolysis Wilson, David B. Current Opinion in Microbiology, Vol. 14, Issue 3 https://doi.org/10.1016/j.mib.2011.04.004	journal	June 2011
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
Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism Kim, S.; Stahlberg, J.; Sandgren, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1316609111	journal	December 2013
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
Crystal Structure and Computational Characterization of the Lytic Polysaccharide Monooxygenase GH61D from the Basidiomycota Fungus Phanerochaete chrysosporium Wu, Miao; Beckham, Gregg T.; Larsson, Anna M. Journal of Biological Chemistry, Vol. 288, Issue 18 https://doi.org/10.1074/jbc.M113.459396	journal	March 2013
Fusion of Dioxygenase and Lignin-binding Domains in a Novel Secreted Enzyme from Cellulolytic Streptomyces sp. SirexAA-E Bianchetti, Christopher M.; Harmann, Connor H.; Takasuka, Taichi E. Journal of Biological Chemistry, Vol. 288, Issue 25 https://doi.org/10.1074/jbc.M113.475848	journal	May 2013
A C4-oxidizing Lytic Polysaccharide Monooxygenase Cleaving Both Cellulose and Cello-oligosaccharides Isaksen, Trine; Westereng, Bjørge; Aachmann, Finn L. Journal of Biological Chemistry, Vol. 289, Issue 5 https://doi.org/10.1074/jbc.M113.530196	journal	December 2013
Crystal Structure and Binding Properties of the Serratia marcescens Chitin-binding Protein CBP21 Vaaje-Kolstad, G.; Houston, D. R.; Riemen, A. H. K. Journal of Biological Chemistry, Vol. 280, Issue 12 https://doi.org/10.1074/jbc.M407175200	journal	December 2004
Understanding the Biological Rationale for the Diversity of Cellulose-directed Carbohydrate-binding Modules in Prokaryotic Enzymes Blake, Anthony W.; McCartney, Lesley; Flint, James E. Journal of Biological Chemistry, Vol. 281, Issue 39 https://doi.org/10.1074/jbc.M605903200	journal	July 2006
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
The novel lectin-like protein CHB1 is encoded by a chitin-inducible Streptomyces olivaceoviridis gene and binds specifically to crystalline ?-chitin of fungi and other organisms Schnellmann, Jürgen; Zeltins, Andris; Blaak, Harald Molecular Microbiology, Vol. 13, Issue 5 https://doi.org/10.1111/j.1365-2958.1994.tb00473.x	journal	September 1994
Cello-Oligosaccharide Oxidation Reveals Differences between Two Lytic Polysaccharide Monooxygenases (Family GH61) from Podospora anserina Bey, Mathieu; Zhou, Simeng; Poidevin, Laetitia Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/AEM.02942-12	journal	November 2012
Oxidoreductive Cellulose Depolymerization by the Enzymes Cellobiose Dehydrogenase and Glycoside Hydrolase 61 Langston, James A.; Shaghasi, Tarana; Abbate, Eric Applied and Environmental Microbiology, Vol. 77, Issue 19, p. 7007-7015 https://doi.org/10.1128/AEM.05815-11	journal	August 2011
Identification of a celE-binding protein and its potential role in induction of the celE gene in Thermomonospora fusca. Lin, E. S.; Wilson, D. B. Journal of Bacteriology, Vol. 170, Issue 9 https://doi.org/10.1128/JB.170.9.3843-3846.1988	journal	January 1988
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577 https://doi.org/10.1128/MMBR.66.3.506-577.2002	journal	September 2002
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 4, p. 739-739 https://doi.org/10.1128/mmbr.66.4.739.2002	journal	December 2002
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014

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Lytic polysaccharide monooxygenase increases cellobiohydrolases activity by promoting decrystallization of cellulose surface

Journal Article · Thu Dec 22 19:00:00 EST 2022 · Science Advances · OSTI ID:1923870

Related Subjects

09 BIOMASS FUELS
AA10
AA9
Biofuels
Biotechnology & Applied Microbiology
Cellulase
Chitinase
Energy & Fuels
Enzyme evolution
LPMO
Lytic polysaccharide monooxygenase
Streptomyces

Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases

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