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Title: Addition of a carbohydrate-binding module enhances cellulase penetration into cellulose substrates

Abstract

Cellulases are of great interest for application in biomass degradation, yet the molecular details of the mode of action of glycoside hydrolases during degradation of insoluble cellulose remain elusive. To further improve these enzymes for application at industrial conditions, it is critical to gain a better understanding of not only the details of the degradation process, but also the function of accessory modules. Method. We fused a carbohydrate-binding module (CBM) from family 2a to two thermophilic endoglucanases. We then applied neutron reflectometry to determine the mechanism of the resulting enhancements. Catalytic activity of the chimeric enzymes was enhanced up to three fold on insoluble cellulose substrates as compared to wild type. Importantly, we demonstrate that the wild type enzymes affect primarily the surface properties of an amorphous cellulose film, while the chimeras containing a CBM alter the bulk properties of the amorphous film. Our findings suggest that the CBM improves the efficiency of these cellulases by enabling digestion within the bulk of the film.

Authors:
 [1];  [2];  [2];  [3];  [4];  [5];  [6];  [2];  [2];  [2];  [4];  [6]
+ Show Author Affiliations
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States)
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
  5. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States)
  6. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )
OSTI Identifier:
1511366
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS

Citation Formats

Reyes-Ortiz, Vimalier, Heins, Richard A., Cheng, Gang, Kim, Edward Y., Vernon, Briana C., Elandt, Ryan B., Adams, Paul D., Sale, Kenneth L., Hadi, Masood Z., Simmons, Blake A., Kent, Michael S., and Tullman-Ercek, Danielle. Addition of a carbohydrate-binding module enhances cellulase penetration into cellulose substrates. United States: N. p., 2013. Web. doi:10.1186/1754-6834-6-93.
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Reyes-Ortiz, Vimalier, Heins, Richard A., Cheng, Gang, Kim, Edward Y., Vernon, Briana C., Elandt, Ryan B., Adams, Paul D., Sale, Kenneth L., Hadi, Masood Z., Simmons, Blake A., Kent, Michael S., & Tullman-Ercek, Danielle. Addition of a carbohydrate-binding module enhances cellulase penetration into cellulose substrates. United States. https://doi.org/10.1186/1754-6834-6-93
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Reyes-Ortiz, Vimalier, Heins, Richard A., Cheng, Gang, Kim, Edward Y., Vernon, Briana C., Elandt, Ryan B., Adams, Paul D., Sale, Kenneth L., Hadi, Masood Z., Simmons, Blake A., Kent, Michael S., and Tullman-Ercek, Danielle. Wed . "Addition of a carbohydrate-binding module enhances cellulase penetration into cellulose substrates". United States. https://doi.org/10.1186/1754-6834-6-93. https://www.osti.gov/servlets/purl/1511366.
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@article{osti_1511366,
title = {Addition of a carbohydrate-binding module enhances cellulase penetration into cellulose substrates},
author = {Reyes-Ortiz, Vimalier and Heins, Richard A. and Cheng, Gang and Kim, Edward Y. and Vernon, Briana C. and Elandt, Ryan B. and Adams, Paul D. and Sale, Kenneth L. and Hadi, Masood Z. and Simmons, Blake A. and Kent, Michael S. and Tullman-Ercek, Danielle},
abstractNote = {Cellulases are of great interest for application in biomass degradation, yet the molecular details of the mode of action of glycoside hydrolases during degradation of insoluble cellulose remain elusive. To further improve these enzymes for application at industrial conditions, it is critical to gain a better understanding of not only the details of the degradation process, but also the function of accessory modules. Method. We fused a carbohydrate-binding module (CBM) from family 2a to two thermophilic endoglucanases. We then applied neutron reflectometry to determine the mechanism of the resulting enhancements. Catalytic activity of the chimeric enzymes was enhanced up to three fold on insoluble cellulose substrates as compared to wild type. Importantly, we demonstrate that the wild type enzymes affect primarily the surface properties of an amorphous cellulose film, while the chimeras containing a CBM alter the bulk properties of the amorphous film. Our findings suggest that the CBM improves the efficiency of these cellulases by enabling digestion within the bulk of the film.},
doi = {10.1186/1754-6834-6-93},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 6,
place = {United States},
year = {Wed Jul 03 00:00:00 EDT 2013},
month = {Wed Jul 03 00:00:00 EDT 2013}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/1754-6834-6-93
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Cited by: 52 works
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Figures / Tables:

Figure 1 Figure 1: Chimeric cellulases (CD-CBM) show higher soluble sugar production from insoluble microcrystalline cellulose (MCC). Two insoluble substrates, microcrystalline cellulose and ionic liquid-pretreated microcrystalline cellulose, were used for this assay. a) Cel9A, Cel9Ako*, Cel9A-CBM, Cel9Ako-CBM*, CBM alone, and Cel9A + CBM untethered; b) Cel5A, Cel5Ako, Cel5A-CBM, Cel5Ako-CBM, CBM alone,more » and Cel5A + CBM untethered. Cellulases were loaded at 200 nM with either 50 mg/ml MCC or IL-MCC at 50°C for 24 h, and DNS assay was used to quantify sugar release with a cellobiose standard curve. *Inactive catalytic domain is indicated with the letters “ko”.« less
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Binding modules alter the activity of chimeric cellulases: Effects of biomass pretreatment and enzyme source
journal, July 2010

  • Kim, Tae-Wan; Chokhawala, Harshal A.; Nadler, Dana
  • Biotechnology and Bioengineering, Vol. 107, Issue 4, p. 601-611
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The challenge of enzyme cost in the production of lignocellulosic biofuels
journal, November 2011

  • Klein-Marcuschamer, Daniel; Oleskowicz-Popiel, Piotr; Simmons, Blake A.
  • Biotechnology and Bioengineering, Vol. 109, Issue 4
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The use of the specular reflection of neutrons to study surfaces and interfaces
book, January 1990

Gene cloning, sequencing, and characterization of a family 9 endoglucanase (CelA) with an unusual pattern of activity from the thermoacidophile Alicyclobacillus acidocaldarius ATCC27009
journal, December 2002

  • K., Eckert; F., Zielinski; Leggio, L. Lo
  • Applied Microbiology and Biotechnology, Vol. 60, Issue 4, p. 428-436
  • DOI: 10.1007/s00253-002-1131-4

Monitoring and Analyzing Process Streams Towards Understanding Ionic Liquid Pretreatment of Switchgrass (Panicum virgatum L.)
journal, April 2010

Cellulase binding to cellulose fibers in high shear fields
journal, July 1994

Applications of computational science for understanding enzymatic deconstruction of cellulose
journal, April 2011

  • Beckham, Gregg T.; Bomble, Yannick J.; Bayer, Edward A.
  • Current Opinion in Biotechnology, Vol. 22, Issue 2
  • DOI: 10.1016/j.copbio.2010.11.005

New polyurethane foams modified with cellulose derivatives
journal, December 2004

Enzymatic degradation of model cellulose films
journal, April 2005

  • Eriksson, Jonny; Malmsten, Martin; Tiberg, Fredrik
  • Journal of Colloid and Interface Science, Vol. 284, Issue 1
  • DOI: 10.1016/j.jcis.2004.10.041

X-ray Crystal Structure of a Non-crystalline Cellulose-specific Carbohydrate-binding Module: CBM28
journal, May 2004

  • Jamal, Sheelan; Nurizzo, Didier; Boraston, Alisdair B.
  • Journal of Molecular Biology, Vol. 339, Issue 2
  • DOI: 10.1016/j.jmb.2004.03.069

Biochemical characterization and crystal structure of endoglucanase Cel5A from the hyperthermophilic Thermotoga maritima
journal, December 2010

  • Pereira, Jose H.; Chen, Zhiwei; McAndrew, Ryan P.
  • Journal of Structural Biology, Vol. 172, Issue 3, p. 372-379
  • DOI: 10.1016/j.jsb.2010.06.018

Selection and optimization of microbial hosts for biofuels production
journal, November 2008

  • Fischer, Curt R.; Klein-Marcuschamer, Daniel; Stephanopoulos, Gregory
  • Metabolic Engineering, Vol. 10, Issue 6, p. 295-304
  • DOI: 10.1016/j.ymben.2008.06.009

Mechanism of interaction between cellulase action and applied shear force, an hypothesis
journal, August 2001

Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959

Characterization of a Thermomonospora fusca exocellulase
journal, March 1995

  • Zhang, Sheng; Lao, Guifang; Wilson, David B.
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  • DOI: 10.1021/bi00010a030

Initial- and Processive-Cut Products Reveal Cellobiohydrolase Rate Limitations and the Role of Companion Enzymes
journal, December 2011

  • Fox, Jerome M.; Levine, Seth E.; Clark, Douglas S.
  • Biochemistry, Vol. 51, Issue 1
  • DOI: 10.1021/bi2011543

Amorphous Characteristics of an Ultrathin Cellulose Film
journal, March 2011

  • Kontturi, Eero; Suchy, Miro; Penttilä, Paavo
  • Biomacromolecules, Vol. 12, Issue 3
  • DOI: 10.1021/bm101382q

Neutron Reflectometry and QCM-D Study of the Interaction of Cellulases with Films of Amorphous Cellulose
journal, June 2011

  • Cheng, Gang; Liu, Zelin; Murton, Jaclyn K.
  • Biomacromolecules, Vol. 12, Issue 6
  • DOI: 10.1021/bm200305u

The Physical Action of Cellulases Revealed by a Quartz Crystal Microbalance Study Using Ultrathin Cellulose Films and Pure Cellulases
journal, January 2008

  • Josefsson, Peter; Henriksson, Gunnar; Wågberg, Lars
  • Biomacromolecules, Vol. 9, Issue 1
  • DOI: 10.1021/bm700980b

Shear Deactivation of Cellulase, Exoglucanase, Endoglucanase, and β-Glucosidase in a Mechanically Agitated Reactor
journal, December 2001

  • Gunjikar, T. P.; Sawant, S. B.; Joshi, J. B.
  • Biotechnology Progress, Vol. 17, Issue 6
  • DOI: 10.1021/bp010114u

Enzymatic Kinetics of Cellulose Hydrolysis:  A QCM-D Study
journal, April 2008

  • Turon, Xavier; Rojas, Orlando J.; Deinhammer, Randall S.
  • Langmuir, Vol. 24, Issue 8
  • DOI: 10.1021/la7032753

A New Lipid Anchor for Sparsely Tethered Bilayer Lipid Membranes †
journal, April 2009

  • Heinrich, Frank; Ng, Tiffany; Vanderah, David J.
  • Langmuir, Vol. 25, Issue 7
  • DOI: 10.1021/la8033275

Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis
journal, January 2010

  • Datta, Supratim; Holmes, Bradley; Park, Joshua I.
  • Green Chemistry, Vol. 12, Issue 2, p. 338-345
  • DOI: 10.1039/b916564a

Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity
journal, May 1998

  • Bolam, David N.; Ciruela, Antonio; McQUEEN-MASON, Simon
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A family of thermostable fungal cellulases created by structure-guided recombination
journal, March 2009

  • Heinzelman, P.; Snow, C. D.; Wu, I.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 14, p. 5610-5615
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Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects
journal, August 2010

  • Herve, C.; Rogowski, A.; Blake, A. W.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 34
  • DOI: 10.1073/pnas.1005732107

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
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CelI, a Noncellulosomal Family 9 Enzyme from Clostridium thermocellum, Is a Processive Endoglucanase That Degrades Crystalline Cellulose
journal, January 2003

The Biological Degradation of Soluble Cellulose Derivatives and its Relationship to the Mechanism of Cellulose Hydrolysis
journal, January 1950

Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis
journal, January 2010

  • Arantes, Valdeir; Saddler, Jack N.
  • Biotechnology for Biofuels, Vol. 3, Issue 1
  • DOI: 10.1186/1754-6834-3-4
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    Impact of Module-X2 and Carbohydrate Binding Module-3 on the catalytic activity of associated glycoside hydrolases towards plant biomass
    journal, June 2017

    Enhanced features of Dictyoglomus turgidum Cellulase A engineered with carbohydrate binding module 11 from Clostridium thermocellum
    journal, March 2018

    Strategies for the production of cell wall-deconstructing enzymes in lignocellulosic biomass and their utilization for biofuel production
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    • Park, Sang-Hyuck; Ong, Rebecca Garlock; Sticklen, Mariam
    • Plant Biotechnology Journal, Vol. 14, Issue 6
    • DOI: 10.1111/pbi.12505

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