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Title: Creation of a functional hyperthermostable designer cellulosome

Abstract

Renewable energy has become a field of high interest over the past decade, and production of biofuels from cellulosic substrates has a particularly high potential as an alternative source of energy. Industrial deconstruction of biomass, however, is an onerous, exothermic process, the cost of which could be decreased significantly by use of hyperthermophilic enzymes. An efficient way of breaking down cellulosic substrates can also be achieved by highly efficient enzymatic complexes called cellulosomes. The modular architecture of these multi-enzyme complexes results in substrate targeting and proximity-based synergy among the resident enzymes. However, cellulosomes have not been observed in hyperthermophilic bacteria. Here, we report the design and function of a novel hyperthermostable “designer cellulosome” system, which is stable and active at 75 °C. Enzymes from Caldicellulosiruptor bescii, a highly cellulolytic hyperthermophilic anaerobic bacterium, were selected and successfully converted to the cellulosomal mode by grafting onto them divergent dockerin modules that can be inserted in a precise manner into a thermostable chimaeric scaffoldin by virtue of their matching cohesins. Three pairs of cohesins and dockerins, selected from thermophilic microbes, were examined for their stability at extreme temperatures and were determined stable at 75 °C for at least 72 h. The resultant hyperthermostablemore » cellulosome complex exhibited the highest levels of enzymatic activity on microcrystalline cellulose at 75 °C, compared to those of previously reported designer cellulosome systems and the native cellulosome from Clostridium thermocellum. The functional hyperthermophilic platform fulfills the appropriate physico-chemical properties required for exothermic processes. This system can thus be adapted for other types of thermostable enzyme systems and could serve as a basis for a variety of cellulolytic and non-cellulolytic industrial objectives at high temperatures.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [4];  [3];  [4];  [4]; ORCiD logo [1]
  1. Weizmann Inst. of Science, Rehovot (Israel). Dept. of Biomolecular Sciences
  2. Weizmann Inst. of Science, Rehovot (Israel). Dept. of Biomolecular Sciences; Ben-Gurion Univ. of the Negev, Beersheba (Israel). Faculty of Natural Sciences
  3. National and Kapodistrian Univ. of Athens (Greece). Microbiology Group. Faculty of Biology
  4. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Weizmann Inst. of Science, Rehovot (Israel); National and Kapodistrian Univ. of Athens (Greece)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); United States—Israel Binational Science Foundation (BSF); Israel Science Foundation (ISF); European Union (EU)
OSTI Identifier:
1502788
Report Number(s):
NREL/JA-2700-73261
Journal ID: ISSN 1754-6834
Grant/Contract Number:  
AC36-08GO28308; 2013284; 1349/13; 604530
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 12; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; multi-enzyme complex; cellulases; thermostability; Caldicellulosiruptor bescii; scaffoldin; dockerin; cohesin

Citation Formats

Kahn, Amaranta, Moraïs, Sarah, Galanopoulou, Anastasia P., Chung, Daehwan, Sarai, Nicholas S., Hengge, Neal, Hatzinikolaou, Dimitris G., Himmel, Michael E., Bomble, Yannick J., and Bayer, Edward A. Creation of a functional hyperthermostable designer cellulosome. United States: N. p., 2019. Web. doi:10.1186/s13068-019-1386-y.
Kahn, Amaranta, Moraïs, Sarah, Galanopoulou, Anastasia P., Chung, Daehwan, Sarai, Nicholas S., Hengge, Neal, Hatzinikolaou, Dimitris G., Himmel, Michael E., Bomble, Yannick J., & Bayer, Edward A. Creation of a functional hyperthermostable designer cellulosome. United States. doi:10.1186/s13068-019-1386-y.
Kahn, Amaranta, Moraïs, Sarah, Galanopoulou, Anastasia P., Chung, Daehwan, Sarai, Nicholas S., Hengge, Neal, Hatzinikolaou, Dimitris G., Himmel, Michael E., Bomble, Yannick J., and Bayer, Edward A. Thu . "Creation of a functional hyperthermostable designer cellulosome". United States. doi:10.1186/s13068-019-1386-y. https://www.osti.gov/servlets/purl/1502788.
@article{osti_1502788,
title = {Creation of a functional hyperthermostable designer cellulosome},
author = {Kahn, Amaranta and Moraïs, Sarah and Galanopoulou, Anastasia P. and Chung, Daehwan and Sarai, Nicholas S. and Hengge, Neal and Hatzinikolaou, Dimitris G. and Himmel, Michael E. and Bomble, Yannick J. and Bayer, Edward A.},
abstractNote = {Renewable energy has become a field of high interest over the past decade, and production of biofuels from cellulosic substrates has a particularly high potential as an alternative source of energy. Industrial deconstruction of biomass, however, is an onerous, exothermic process, the cost of which could be decreased significantly by use of hyperthermophilic enzymes. An efficient way of breaking down cellulosic substrates can also be achieved by highly efficient enzymatic complexes called cellulosomes. The modular architecture of these multi-enzyme complexes results in substrate targeting and proximity-based synergy among the resident enzymes. However, cellulosomes have not been observed in hyperthermophilic bacteria. Here, we report the design and function of a novel hyperthermostable “designer cellulosome” system, which is stable and active at 75 °C. Enzymes from Caldicellulosiruptor bescii, a highly cellulolytic hyperthermophilic anaerobic bacterium, were selected and successfully converted to the cellulosomal mode by grafting onto them divergent dockerin modules that can be inserted in a precise manner into a thermostable chimaeric scaffoldin by virtue of their matching cohesins. Three pairs of cohesins and dockerins, selected from thermophilic microbes, were examined for their stability at extreme temperatures and were determined stable at 75 °C for at least 72 h. The resultant hyperthermostable cellulosome complex exhibited the highest levels of enzymatic activity on microcrystalline cellulose at 75 °C, compared to those of previously reported designer cellulosome systems and the native cellulosome from Clostridium thermocellum. The functional hyperthermophilic platform fulfills the appropriate physico-chemical properties required for exothermic processes. This system can thus be adapted for other types of thermostable enzyme systems and could serve as a basis for a variety of cellulolytic and non-cellulolytic industrial objectives at high temperatures.},
doi = {10.1186/s13068-019-1386-y},
journal = {Biotechnology for Biofuels},
number = ,
volume = 12,
place = {United States},
year = {2019},
month = {2}
}

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Cited by: 6 works
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    Works referencing / citing this record:

    Studies ofThermobifida fusca plant cell wall degrading enzymes
    journal, January 2004


    Description of Caldicellulosiruptor saccharolyticus gen. nov., sp. nov: An obligately anaerobic, extremely thermophilic, cellulolytic bacterium
    journal, July 1994


    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
    • DOI: 10.1128/aem.01400-10

    Expression, purification and subunit-binding properties of cohesins 2 and 3 of the Clostridium thermocellum cellulosome
    journal, February 1995


    Significance of Relative Position of Cellulases in Designer Cellulosomes for Optimized Cellulolysis
    journal, May 2015


    Affinity digestion for the near-total recovery of purified cellulosome from Clostridium thermocellum
    journal, April 1992

    • Morag (Morgenstern), Ely; Bayer, Edward A.; Lamed, Raphael
    • Enzyme and Microbial Technology, Vol. 14, Issue 4
    • DOI: 10.1016/0141-0229(92)90153-f

    celA, another gene coding for a multidomain cellulase from the extreme thermophile Caldocellum saccharolyticum
    journal, June 1995

    • Te'o, V. S. J.; Saul, D. J.; Bergquist, P. L.
    • Applied Microbiology and Biotechnology, Vol. 43, Issue 2
    • DOI: 10.1007/bf00172827

    Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca
    journal, October 1997

    • Sakon, Joshua; Irwin, Diana; Wilson, David B.
    • Nature Structural Biology, Vol. 4, Issue 10
    • DOI: 10.1038/nsb1097-810

    Enhancement of cellulosome-mediated deconstruction of cellulose by improving enzyme thermostability
    journal, August 2016


    Herbivorax saccincola gen. nov., sp. nov., a cellulolytic, anaerobic, thermophilic bacterium isolated via in sacco enrichments from a lab-scale biogas reactor
    journal, November 2016

    • Koeck, Daniela E.; Mechelke, Matthias; Zverlov, Vladimir V.
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 11
    • DOI: 10.1099/ijsem.0.001374

    The Multi Domain Caldicellulosiruptor bescii CelA Cellulase Excels at the Hydrolysis of Crystalline Cellulose
    journal, August 2017


    Use of Label-Free Quantitative Proteomics To Distinguish the Secreted Cellulolytic Systems of Caldicellulosiruptor bescii and Caldicellulosiruptor obsidiansis
    journal, April 2011

    • Lochner, Adriane; Giannone, Richard J.; Rodriguez, Miguel
    • Applied and Environmental Microbiology, Vol. 77, Issue 12
    • DOI: 10.1128/aem.02811-10

    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
    • DOI: 10.1186/s13068-018-1014-2

    Enzyme recycling in lignocellulosic biorefineries
    journal, October 2016

    • Jørgensen, Henning; Pinelo, Manuel
    • Biofuels, Bioproducts and Biorefining, Vol. 11, Issue 1
    • DOI: 10.1002/bbb.1724

    Toward combined delignification and saccharification of wheat straw by a laccase-containing designer cellulosome
    journal, September 2016

    • Davidi, Lital; Moraïs, Sarah; Artzi, Lior
    • Proceedings of the National Academy of Sciences, Vol. 113, Issue 39
    • DOI: 10.1073/pnas.1608012113

    A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates
    journal, January 2013


    Adaptor Scaffoldins: An Original Strategy for Extended Designer Cellulosomes, Inspired from Nature
    journal, April 2016


    Cellulosomes and designer cellulosomes: why toy with Nature?: Crystal ball
    journal, November 2016


    Nanoscale Engineering of Designer Cellulosomes
    journal, January 2016

    • Gunnoo, Melissabye; Cazade, Pierre-André; Galera-Prat, Albert
    • Advanced Materials, Vol. 28, Issue 27
    • DOI: 10.1002/adma.201503948

    Improved Thermostability of Clostridium thermocellum Endoglucanase Cel8A by Using Consensus-Guided Mutagenesis
    journal, March 2012

    • Anbar, Michael; Gul, Ozgur; Lamed, Raphael
    • Applied and Environmental Microbiology, Vol. 78, Issue 9
    • DOI: 10.1128/aem.07985-11

    Conversion of Thermobifida fusca free exoglucanases into cellulosomal components: Comparative impact on cellulose-degrading activity
    journal, July 2008


    Abundance and Diversity of Dockerin-Containing Proteins in the Fiber-Degrading Rumen Bacterium, Ruminococcus flavefaciens FD-1
    journal, August 2010


    Thermostability Enhancement of Clostridium thermocellum Cellulosomal Endoglucanase Cel8A by a Single Glycine Substitution
    journal, July 2010


    Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
    journal, February 2007

    • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
    • Science, Vol. 315, Issue 5813, p. 804-807
    • DOI: 10.1126/science.1137016

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