Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species
Abstract
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.
- Authors:
-
- North Carolina State Univ., Raleigh, NC (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Univ. of Georgia, Athens, GA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1475518
- Alternate Identifier(s):
- OSTI ID: 1464583
- Report Number(s):
- NREL/JA-2700-71961
Journal ID: ISSN 0001-1541
- Grant/Contract Number:
- AC36-08GO28308; P200A160061; P200A100004-12; GM008776‐11
- Resource Type:
- Accepted Manuscript
- Journal Name:
- AIChE Journal
- Additional Journal Information:
- Journal Volume: 64; Journal Issue: 12; Journal ID: ISSN 0001-1541
- Publisher:
- American Institute of Chemical Engineers
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; Caldicellulosiruptor; lignocellulose; glycoside hydrolase; cellulase
Citation Formats
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., and Kelly, Robert M. Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species. United States: N. p., 2018.
Web. doi:10.1002/aic.16354.
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. Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species. United States. https://doi.org/10.1002/aic.16354
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., and Kelly, Robert M. Wed .
"Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species". United States. https://doi.org/10.1002/aic.16354. https://www.osti.gov/servlets/purl/1475518.
@article{osti_1475518,
title = {Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species},
author = {Conway, Jonathan M. and Crosby, James R. and Hren, Andrew P. and Southerland, Robert T. and Lee, Laura L. and Lunin, Vladimir V. and Alahuhta, Petri and Himmel, Michael E. and Bomble, Yannick J. and Adams, Michael W. W. and Kelly, Robert M.},
abstractNote = {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.},
doi = {10.1002/aic.16354},
journal = {AIChE Journal},
number = 12,
volume = 64,
place = {United States},
year = {2018},
month = {7}
}
Web of Science
Works referenced in this record:
S-Layer Homology Domain Proteins Csac_0678 and Csac_2722 Are Implicated in Plant Polysaccharide Deconstruction by the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus
journal, December 2011
- Ozdemir, Inci; Blumer-Schuette, Sara E.; Kelly, Robert M.
- Applied and Environmental Microbiology, Vol. 78, Issue 3
High activity CAZyme cassette for improving biomass degradation in thermophiles
journal, February 2018
- Brunecky, Roman; Chung, Daehwan; Sarai, Nicholas S.
- Biotechnology for Biofuels, Vol. 11, Issue 1
Genus-Wide Assessment of Lignocellulose Utilization in the Extremely Thermophilic Genus Caldicellulosiruptor by Genomic, Pangenomic, and Metagenomic Analyses
journal, February 2018
- Lee, Laura L.; Blumer-Schuette, Sara E.; Izquierdo, Javier A.
- Applied and Environmental Microbiology, Vol. 84, Issue 9
A Highly Thermostable Kanamycin Resistance Marker Expands the Tool Kit for Genetic Manipulation of Caldicellulosiruptor bescii
journal, May 2016
- Lipscomb, Gina L.; Conway, Jonathan M.; Blumer-Schuette, Sara E.
- Applied and Environmental Microbiology, Vol. 82, Issue 14
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
The N-Terminal GH10 Domain of a Multimodular Protein from Caldicellulosiruptor bescii Is a Versatile Xylanase/β-Glucanase That Can Degrade Crystalline Cellulose
journal, March 2015
- Xue, Xianli; Wang, Rong; Tu, Tao
- Applied and Environmental Microbiology, Vol. 81, Issue 11
Caldicellulosiruptor Core and Pangenomes Reveal Determinants for Noncellulosomal Thermophilic Deconstruction of Plant Biomass
journal, May 2012
- Blumer-Schuette, S. E.; Giannone, R. J.; Zurawski, J. V.
- Journal of Bacteriology, Vol. 194, Issue 15
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements
journal, June 2004
- Darling, A. C. E.
- Genome Research, Vol. 14, Issue 7
Multidomain, Surface Layer-associated Glycoside Hydrolases Contribute to Plant Polysaccharide Degradation by Caldicellulosiruptor Species
journal, January 2016
- Conway, Jonathan M.; Pierce, William S.; Le, Jaycee H.
- Journal of Biological Chemistry, Vol. 291, Issue 13
Parsing in vivo and in vitro contributions to microcrystalline cellulose hydrolysis by multidomain glycoside hydrolases in the Caldicellulosiruptor bescii secretome
journal, July 2018
- Conway, Jonathan M.; Crosby, James R.; McKinley, Bennett S.
- Biotechnology and Bioengineering, Vol. 115, Issue 10
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions
journal, November 2004
- Krissinel, E.; Henrick, K.
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12
Comparative Community Proteomics Demonstrates the Unexpected Importance of Actinobacterial Glycoside Hydrolase Family 12 Protein for Crystalline Cellulose Hydrolysis
journal, August 2016
- Hiras, Jennifer; Wu, Yu-Wei; Deng, Kai
- mBio, Vol. 7, Issue 4
Thermophilic lignocellulose deconstruction
journal, May 2014
- Blumer-Schuette, Sara E.; Brown, Steven D.; Sander, Kyle B.
- FEMS Microbiology Reviews, Vol. 38, Issue 3
Fine-structural variance of family 3 carbohydrate-binding modules as extracellular biomass-sensing components of Clostridium thermocellum anti-σ I factors
journal, January 2014
- Yaniv, Oren; Fichman, Galit; Borovok, Ilya
- Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 2
Complete Genome Sequences of Caldicellulosiruptor sp. Strain Rt8.B8, Caldicellulosiruptor sp. Strain Wai35.B1, and “ Thermoanaerobacter cellulolyticus ”
journal, May 2015
- Lee, Laura L.; Izquierdo, Javier A.; Blumer-Schuette, Sara E.
- Genome Announcements, Vol. 3, Issue 3
Measurement of cellulase activities
journal, January 1987
- Ghose, T. K.
- Pure and Applied Chemistry, Vol. 59, Issue 2
Phylogenetic, Microbiological, and Glycoside Hydrolase Diversities within the Extremely Thermophilic, Plant Biomass-Degrading Genus Caldicellulosiruptor
journal, October 2010
- Blumer-Schuette, S. E.; Lewis, D. L.; Kelly, R. M.
- Applied and Environmental Microbiology, Vol. 76, Issue 24, p. 8084-8092
Identification of the C-Terminal GH5 Domain from CbCel9B/Man5A as the First Glycoside Hydrolase with Thermal Activation Property from a Multimodular Bifunctional Enzyme
journal, June 2016
- Wang, Rong; Gong, Li; Xue, Xianli
- PLOS ONE, Vol. 11, Issue 6
Functional Analysis of the Glucan Degradation Locus in Caldicellulosiruptor bescii Reveals Essential Roles of Component Glycoside Hydrolases in Plant Biomass Deconstruction
journal, October 2017
- Conway, Jonathan M.; McKinley, Bennett S.; Seals, Nathaniel L.
- Applied and Environmental Microbiology, Vol. 83, Issue 24
Methylation by a Unique α-class N4-Cytosine Methyltransferase Is Required for DNA Transformation of Caldicellulosiruptor bescii DSM6725
journal, August 2012
- Chung, Daehwan; Farkas, Joel; Huddleston, Jennifer R.
- PLoS ONE, Vol. 7, Issue 8
Genome Stability in Engineered Strains of the Extremely Thermophilic Lignocellulose-Degrading Bacterium Caldicellulosiruptor bescii
journal, May 2017
- Williams-Rhaesa, Amanda M.; Poole, Farris L.; Dinsmore, Jessica T.
- Applied and Environmental Microbiology, Vol. 83, Issue 14
Accurate bond and angle parameters for X-ray protein structure refinement
journal, July 1991
- Engh, R. A.; Huber, R.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 4
Improving the quality of twilight-zone alignments
journal, January 2000
- Jaroszewski, Lukasz; Godzik, Adam; Rychlewski, Leszek
- Protein Science, Vol. 9, Issue 8
Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus
journal, March 2011
- VanFossen, Amy L.; Ozdemir, Inci; Zelin, Samantha L.
- Biotechnology and Bioengineering, Vol. 108, Issue 7
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
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959
- Miller, G. L.
- Analytical Chemistry, Vol. 31, Issue 3
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Comparison of sequence profiles. Strategies for structural predictions using sequence information
journal, January 2000
- Rychlewski, Leszek; Li, Weizhong; Jaroszewski, Lukasz
- Protein Science, Vol. 9, Issue 2
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii
journal, June 2014
- Chung, D.; Cha, M.; Guss, A. M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 24, p. 8931-8936
Protein production by auto-induction in high-density shaking cultures
journal, May 2005
- Studier, F. William
- Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234
Characterization of the Four GH12 Endoxylanases from the Plant Pathogen Fusarium graminearum
journal, August 2012
- Habrylo, Olivier
- Journal of Microbiology and Biotechnology, Vol. 22, Issue 8
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA
journal, December 2013
- Brunecky, R.; Alahuhta, M.; Xu, Q.
- Science, Vol. 342, Issue 6165, p. 1513-1516
FFAS03: a server for profile-profile sequence alignments
journal, July 2005
- Jaroszewski, L.; Rychlewski, L.; Li, Z.
- Nucleic Acids Research, Vol. 33, Issue Web Server
A graph-theory algorithm for rapid protein side-chain prediction
journal, September 2003
- Canutescu, Adrian A.; Shelenkov, Andrew A.; Dunbrack, Roland L.
- Protein Science, Vol. 12, Issue 9
Stability of domain structures in multi-domain proteins
journal, July 2011
- Bhaskara, Ramachandra M.; Srinivasan, Narayanaswamy
- Scientific Reports, Vol. 1, Issue 1
Native xylose-inducible promoter expands the genetic tools for the biomass-degrading, extremely thermophilic bacterium Caldicellulosiruptor bescii
journal, May 2018
- Williams-Rhaesa, Amanda M.; Awuku, Nanaakua K.; Lipscomb, Gina L.
- Extremophiles, Vol. 22, Issue 4
The renaissance of life near the boiling point - at last, genetics and metabolic engineering
journal, December 2016
- Adams, Michael W. W.; Kelly, Robert M.
- Microbial Biotechnology, Vol. 10, Issue 1
Molecular and Biochemical Analyses of CbCel9A/Cel48A, a Highly Secreted Multi-Modular Cellulase by Caldicellulosiruptor bescii during Growth on Crystalline Cellulose
journal, December 2013
- Yi, Zhuolin; Su, Xiaoyun; Revindran, Vanessa
- PLoS ONE, Vol. 8, Issue 12
Molecular replacement with MOLREP
journal, December 2009
- Vagin, Alexei; Teplyakov, Alexei
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
Biochemical and Mutational Analyses of a Multidomain Cellulase/Mannanase from Caldicellulosiruptor bescii
journal, January 2012
- Su, Xiaoyun; Mackie, Roderick I.; Cann, Isaac K. O.
- Applied and Environmental Microbiology, Vol. 78, Issue 7
Homologous Expression of the Caldicellulosiruptor bescii CelA Reveals that the Extracellular Protein Is Glycosylated
journal, March 2015
- Chung, Daehwan; Young, Jenna; Bomble, Yannick J.
- PLOS ONE, Vol. 10, Issue 3
Multidomain and Multifunctional Glycosyl Hydrolases from the Extreme Thermophile Caldicellulosiruptor Isolate Tok7B.1
journal, May 2000
- Gibbs, Moreland D.; Reeves, Rosalind A.; Farrington, G. King
- Current Microbiology, Vol. 40, Issue 5, p. 333-340
Structural Insights into the Specificity of Xyn10B from Paenibacillus barcinonensis and Its Improved Stability by Forced Protein Evolution
journal, November 2009
- Gallardo, Óscar; Pastor, F. I. Javier; Polaina, Julio
- Journal of Biological Chemistry, Vol. 285, Issue 4
Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals
journal, November 2015
- Zeldes, Benjamin M.; Keller, Matthew W.; Loder, Andrew J.
- Frontiers in Microbiology, Vol. 6
Overcoming restriction as a barrier to DNA transformation in Caldicellulosiruptor species results in efficient marker replacement
journal, January 2013
- Chung, Daehwan; Farkas, Joel; Westpheling, Janet
- Biotechnology for Biofuels, Vol. 6, Issue 1
Molecular and Biochemical Analyses of the GH44 Module of CbMan5B/Cel44A, a Bifunctional Enzyme from the Hyperthermophilic Bacterium Caldicellulosiruptor bescii
journal, July 2012
- Ye, Libin; Su, Xiaoyun; Schmitz, George E.
- Applied and Environmental Microbiology, Vol. 78, Issue 19
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen
journal, August 2020
- Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe
- JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
An optimized growth medium for increased recombinant protein secretion titer via the type III secretion system
journal, February 2021
- Burdette, Lisa Ann; Wong, Han Teng; Tullman-Ercek, Danielle
- Microbial Cell Factories, Vol. 20, Issue 1
Consolidated bioprocessing of lignocellulose for production of glucaric acid by an artificial microbial consortium
journal, April 2021
- Li, Chaofeng; Lin, Xiaofeng; Ling, Xing
- Biotechnology for Biofuels, Vol. 14, Issue 1
Overview of the CCP4 suite and current developments.
text, January 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Apollo - University of Cambridge Repository
The Protein Data Bank
journal, May 2002
- Berman, Helen M.; Battistuz, Tammy; Bhat, T. N.
- Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 6
Works referencing / citing this record:
The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan
journal, December 2019
- Chu, Yindi; Hao, Zhenzhen; Wang, Kaikai
- Biotechnology for Biofuels, Vol. 12, Issue 1
Genomic and physiological analyses reveal that extremely thermophilic Caldicellulosiruptor changbaiensis deploys uncommon cellulose attachment mechanisms
journal, August 2019
- Khan, Asma M. A. M.; Mendoza, Carl; Hauk, Valerie J.
- Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10