Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species

Conway, Jonathan M.; Crosby, James R.; Hren, Andrew P.; Southerland, Robert T.; Lee, Laura L.; Lunin, Vladimir V.; Alahuhta, Petri; Himmel, Michael E.; Bomble, Yannick J.; Adams, Michael W.  W.; Kelly, Robert M.

doi:10.1002/aic.16354

Title: Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species

Journal Article · 11 July 2018 · AIChE Journal

DOI: https://doi.org/10.1002/aic.16354 · OSTI ID:1475518

Conway, Jonathan M. ^[1]; Crosby, James R. ^[1]; Hren, Andrew P. ^[1]; Southerland, Robert T. ^[1]; Lee, Laura L. ^[1]; Lunin, Vladimir V. ^[2]; Alahuhta, Petri ^[2]; Himmel, Michael E. ^[2]; Bomble, Yannick J. ^[2]; Adams, Michael W. W. ^[3];

^[1]

North Carolina State Univ., Raleigh, NC (United States)
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Univ. of Georgia, Athens, GA (United States)

Biological hydrolysis of microcrystalline cellulose is an uncommon feature in the microbial world, especially among bacteria and archaea growing optimally above 70 degrees C (the so-called extreme thermophiles). In fact, among this group only certain species in the genus Caldicellulosiruptor are capable of rapid and extensive cellulose degradation. Four novel multidomain glycoside hydrolases (GHs) from Caldicellulosiruptor morganii and Caldicellulosiruptor danielii were produced recombinantly in Caldicellulosiruptor bescii and characterized. These GHs are structurally organized with two or three catalytic domains flanking carbohydrate binding modules from Family 3. Collectively, these enzymes represent GH families 5, 9, 10, 12, 44, 48, and 74, and hydrolyze crystalline cellulose, glucan, xylan, and mannan, the primary carbohydrates in plant biomass. Degradation of microcrystalline cellulose by cocktails of GHs from three Caldicellulosiruptor species demonstrated that synergistic interactions enable mixtures of multiple enzymes to outperform single enzymes, suggesting a community mode of action for lignocellulose utilization in thermal environments.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC36-08GO28308; P200A160061; P200A100004-12; GM008776‐11

OSTI ID:: 1475518

Alternate ID(s):: OSTI ID: 1464583

Report Number(s):: NREL/JA-2700-71961

Journal Information:: AIChE Journal, Vol. 64, Issue 12; ISSN 0001-1541

Publisher:: American Institute of Chemical EngineersCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (54)

S-Layer Homology Domain Proteins Csac_0678 and Csac_2722 Are Implicated in Plant Polysaccharide Deconstruction by the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus Ozdemir, Inci; Blumer-Schuette, Sara E.; Kelly, Robert M. Applied and Environmental Microbiology, Vol. 78, Issue 3 https://doi.org/10.1128/AEM.07031-11	journal	December 2011
High activity CAZyme cassette for improving biomass degradation in thermophiles Brunecky, Roman; Chung, Daehwan; Sarai, Nicholas S. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1014-2	journal	February 2018
Genus-Wide Assessment of Lignocellulose Utilization in the Extremely Thermophilic Genus Caldicellulosiruptor by Genomic, Pangenomic, and Metagenomic Analyses Lee, Laura L.; Blumer-Schuette, Sara E.; Izquierdo, Javier A. Applied and Environmental Microbiology, Vol. 84, Issue 9 https://doi.org/10.1128/AEM.02694-17	journal	February 2018
A Highly Thermostable Kanamycin Resistance Marker Expands the Tool Kit for Genetic Manipulation of Caldicellulosiruptor bescii Lipscomb, Gina L.; Conway, Jonathan M.; Blumer-Schuette, Sara E. Applied and Environmental Microbiology, Vol. 82, Issue 14 https://doi.org/10.1128/AEM.00570-16	journal	May 2016
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
The N-Terminal GH10 Domain of a Multimodular Protein from Caldicellulosiruptor bescii Is a Versatile Xylanase/β-Glucanase That Can Degrade Crystalline Cellulose Xue, Xianli; Wang, Rong; Tu, Tao Applied and Environmental Microbiology, Vol. 81, Issue 11 https://doi.org/10.1128/AEM.00432-15	journal	March 2015
Caldicellulosiruptor Core and Pangenomes Reveal Determinants for Noncellulosomal Thermophilic Deconstruction of Plant Biomass Blumer-Schuette, S. E.; Giannone, R. J.; Zurawski, J. V. Journal of Bacteriology, Vol. 194, Issue 15 https://doi.org/10.1128/JB.00266-12	journal	May 2012
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements Darling, A. C. E. Genome Research, Vol. 14, Issue 7 https://doi.org/10.1101/gr.2289704	journal	June 2004
Multidomain, Surface Layer-associated Glycoside Hydrolases Contribute to Plant Polysaccharide Degradation by Caldicellulosiruptor Species Conway, Jonathan M.; Pierce, William S.; Le, Jaycee H. Journal of Biological Chemistry, Vol. 291, Issue 13 https://doi.org/10.1074/jbc.M115.707810	journal	January 2016
Parsing in vivo and in vitro contributions to microcrystalline cellulose hydrolysis by multidomain glycoside hydrolases in the Caldicellulosiruptor bescii secretome Conway, Jonathan M.; Crosby, James R.; McKinley, Bennett S. Biotechnology and Bioengineering, Vol. 115, Issue 10 https://doi.org/10.1002/bit.26773	journal	July 2018
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
Comparative Community Proteomics Demonstrates the Unexpected Importance of Actinobacterial Glycoside Hydrolase Family 12 Protein for Crystalline Cellulose Hydrolysis Hiras, Jennifer; Wu, Yu-Wei; Deng, Kai mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.01106-16	journal	August 2016
Thermophilic lignocellulose deconstruction Blumer-Schuette, Sara E.; Brown, Steven D.; Sander, Kyle B. FEMS Microbiology Reviews, Vol. 38, Issue 3 https://doi.org/10.1111/1574-6976.12044	journal	May 2014
Fine-structural variance of family 3 carbohydrate-binding modules as extracellular biomass-sensing components of Clostridium thermocellum anti-σ ^I factors Yaniv, Oren; Fichman, Galit; Borovok, Ilya Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 2 https://doi.org/10.1107/S139900471302926X	journal	January 2014
Complete Genome Sequences of Caldicellulosiruptor sp. Strain Rt8.B8, Caldicellulosiruptor sp. Strain Wai35.B1, and “ Thermoanaerobacter cellulolyticus ” Lee, Laura L.; Izquierdo, Javier A.; Blumer-Schuette, Sara E. Genome Announcements, Vol. 3, Issue 3 https://doi.org/10.1128/genomeA.00440-15	journal	May 2015
Measurement of cellulase activities Ghose, T. K. Pure and Applied Chemistry, Vol. 59, Issue 2 https://doi.org/10.1351/pac198759020257	journal	January 1987
Phylogenetic, Microbiological, and Glycoside Hydrolase Diversities within the Extremely Thermophilic, Plant Biomass-Degrading Genus Caldicellulosiruptor Blumer-Schuette, S. E.; Lewis, D. L.; Kelly, R. M. Applied and Environmental Microbiology, Vol. 76, Issue 24, p. 8084-8092 https://doi.org/10.1128/AEM.01400-10	journal	October 2010
Identification of the C-Terminal GH5 Domain from CbCel9B/Man5A as the First Glycoside Hydrolase with Thermal Activation Property from a Multimodular Bifunctional Enzyme Wang, Rong; Gong, Li; Xue, Xianli PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156802	journal	June 2016
Functional Analysis of the Glucan Degradation Locus in Caldicellulosiruptor bescii Reveals Essential Roles of Component Glycoside Hydrolases in Plant Biomass Deconstruction Conway, Jonathan M.; McKinley, Bennett S.; Seals, Nathaniel L. Applied and Environmental Microbiology, Vol. 83, Issue 24 https://doi.org/10.1128/AEM.01828-17	journal	October 2017
Methylation by a Unique α-class N4-Cytosine Methyltransferase Is Required for DNA Transformation of Caldicellulosiruptor bescii DSM6725 Chung, Daehwan; Farkas, Joel; Huddleston, Jennifer R. PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0043844	journal	August 2012
Genome Stability in Engineered Strains of the Extremely Thermophilic Lignocellulose-Degrading Bacterium Caldicellulosiruptor bescii Williams-Rhaesa, Amanda M.; Poole, Farris L.; Dinsmore, Jessica T. Applied and Environmental Microbiology, Vol. 83, Issue 14 https://doi.org/10.1128/AEM.00444-17	journal	May 2017
Accurate bond and angle parameters for X-ray protein structure refinement Engh, R. A.; Huber, R. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S0108767391001071	journal	July 1991
Improving the quality of twilight-zone alignments Jaroszewski, Lukasz; Godzik, Adam; Rychlewski, Leszek Protein Science, Vol. 9, Issue 8 https://doi.org/10.1110/ps.9.8.1487	journal	January 2000
Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus VanFossen, Amy L.; Ozdemir, Inci; Zelin, Samantha L. Biotechnology and Bioengineering, Vol. 108, Issue 7 https://doi.org/10.1002/bit.23093	journal	March 2011
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar Miller, G. L. Analytical Chemistry, Vol. 31, Issue 3 https://doi.org/10.1021/ac60147a030	journal	March 1959
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Comparison of sequence profiles. Strategies for structural predictions using sequence information Rychlewski, Leszek; Li, Weizhong; Jaroszewski, Lukasz Protein Science, Vol. 9, Issue 2 https://doi.org/10.1110/ps.9.2.232	journal	January 2000
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii Chung, D.; Cha, M.; Guss, A. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 24, p. 8931-8936 https://doi.org/10.1073/pnas.1402210111	journal	June 2014
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Characterization of the Four GH12 Endoxylanases from the Plant Pathogen Fusarium graminearum Habrylo, Olivier Journal of Microbiology and Biotechnology, Vol. 22, Issue 8 https://doi.org/10.4014/jmb.1112.11019	journal	August 2012
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA Brunecky, R.; Alahuhta, M.; Xu, Q. Science, Vol. 342, Issue 6165, p. 1513-1516 https://doi.org/10.1126/science.1244273	journal	December 2013
FFAS03: a server for profile-profile sequence alignments Jaroszewski, L.; Rychlewski, L.; Li, Z. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki418	journal	July 2005
A graph-theory algorithm for rapid protein side-chain prediction Canutescu, Adrian A.; Shelenkov, Andrew A.; Dunbrack, Roland L. Protein Science, Vol. 12, Issue 9 https://doi.org/10.1110/ps.03154503	journal	September 2003
Stability of domain structures in multi-domain proteins Bhaskara, Ramachandra M.; Srinivasan, Narayanaswamy Scientific Reports, Vol. 1, Issue 1 https://doi.org/10.1038/srep00040	journal	July 2011
Native xylose-inducible promoter expands the genetic tools for the biomass-degrading, extremely thermophilic bacterium Caldicellulosiruptor bescii Williams-Rhaesa, Amanda M.; Awuku, Nanaakua K.; Lipscomb, Gina L. Extremophiles, Vol. 22, Issue 4 https://doi.org/10.1007/s00792-018-1023-x	journal	May 2018
The renaissance of life near the boiling point - at last, genetics and metabolic engineering Adams, Michael W. W.; Kelly, Robert M. Microbial Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1111/1751-7915.12463	journal	December 2016
Enzymatic Assembly of Overlapping DNA Fragments Gibson, Daniel G. Methods in Enzymology https://doi.org/10.1016/B978-0-12-385120-8.00015-2	book	May 2011
Molecular and Biochemical Analyses of CbCel9A/Cel48A, a Highly Secreted Multi-Modular Cellulase by Caldicellulosiruptor bescii during Growth on Crystalline Cellulose Yi, Zhuolin; Su, Xiaoyun; Revindran, Vanessa PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0084172	journal	December 2013
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042589	journal	December 2009
Biochemical and Mutational Analyses of a Multidomain Cellulase/Mannanase from Caldicellulosiruptor bescii Su, Xiaoyun; Mackie, Roderick I.; Cann, Isaac K. O. Applied and Environmental Microbiology, Vol. 78, Issue 7 https://doi.org/10.1128/AEM.06814-11	journal	January 2012
Homologous Expression of the Caldicellulosiruptor bescii CelA Reveals that the Extracellular Protein Is Glycosylated Chung, Daehwan; Young, Jenna; Bomble, Yannick J. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0119508	journal	March 2015
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Multidomain and Multifunctional Glycosyl Hydrolases from the Extreme Thermophile Caldicellulosiruptor Isolate Tok7B.1 Gibbs, Moreland D.; Reeves, Rosalind A.; Farrington, G. King Current Microbiology, Vol. 40, Issue 5, p. 333-340 https://doi.org/10.1007/s002849910066	journal	May 2000
Structural Insights into the Specificity of Xyn10B from Paenibacillus barcinonensis and Its Improved Stability by Forced Protein Evolution Gallardo, Óscar; Pastor, F. I. Javier; Polaina, Julio Journal of Biological Chemistry, Vol. 285, Issue 4 https://doi.org/10.1074/jbc.M109.064394	journal	November 2009
Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals Zeldes, Benjamin M.; Keller, Matthew W.; Loder, Andrew J. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01209	journal	November 2015
Overcoming restriction as a barrier to DNA transformation in Caldicellulosiruptor species results in efficient marker replacement Chung, Daehwan; Farkas, Joel; Westpheling, Janet Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-82	journal	January 2013
Molecular and Biochemical Analyses of the GH44 Module of CbMan5B/Cel44A, a Bifunctional Enzyme from the Hyperthermophilic Bacterium Caldicellulosiruptor bescii Ye, Libin; Su, Xiaoyun; Schmitz, George E. Applied and Environmental Microbiology, Vol. 78, Issue 19 https://doi.org/10.1128/AEM.02009-12	journal	July 2012
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
An optimized growth medium for increased recombinant protein secretion titer via the type III secretion system Burdette, Lisa Ann; Wong, Han Teng; Tullman-Ercek, Danielle Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01536-z	journal	February 2021
Consolidated bioprocessing of lignocellulose for production of glucaric acid by an artificial microbial consortium Li, Chaofeng; Lin, Xiaofeng; Ling, Xing Biotechnology for Biofuels, Vol. 14, Issue 1 https://doi.org/10.1186/s13068-021-01961-7	journal	April 2021
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011

Cited By (3)

The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan Chu, Yindi; Hao, Zhenzhen; Wang, Kaikai Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1617-2	journal	December 2019
Genomic and physiological analyses reveal that extremely thermophilic Caldicellulosiruptor changbaiensis deploys uncommon cellulose attachment mechanisms Khan, Asma M. A. M.; Mendoza, Carl; Hauk, Valerie J. Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10 https://doi.org/10.1007/s10295-019-02222-1	journal	August 2019
The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan Chu, Yindi; Hao, Zhenzhen; Wang, Kaikai Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1617-2	journal	December 2019

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Title: Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species

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