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Title: Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass

Abstract

Background: Enzymatic hydrolysis of pretreated lignocellulosic biomass is an essential process for the production of fermentable sugars for industrial use. A better understanding of fungal cellulase systems will provide clues for maximizing the hydrolysis of target biomass. Talaromyces cellulolyticus is a promising fungus for cellulase production and efficient biomass hydrolysis. Several cellulolytic enzymes purified from T. cellulolyticus were characterized in earlier studies, but the core enzymes critical for hydrolysis of lignocellulosic biomass remain unknown. Results: Six cellulolytic enzymes critical for the hydrolysis of crystalline cellulose were purified from T. cellulolyticus culture supernatant using an enzyme assay based on synergistic hydrolysis of Avicel. The purified enzymes were identified by their substrate specificities and analyses of trypsin-digested peptide fragments and were classified into the following glycosyl hydrolase (GH) families: GH3 (β-glucosidase, Bgl3A), GH5 (endoglucanase, Cel5A), GH6 (cellobiohydrolase II, Cel6A), GH7 (cellobiohydrolase I and endoglucanase, Cel7A and Cel7B, respectively), and GH10 (xylanase, Xyl10A). Hydrolysis of dilute acid-pretreated corn stover (PCS) with mixtures of the purified enzymes showed that Cel5A, Cel7B, and Xyl10A each had synergistic effects with a mixture of Cel6A and Cel7A. Cel5A seemed to be more effective in the synergistic hydrolysis of the PCS than Cel7B. The ratio of Cel5A, Cel6A,more » Cel7A, and Xyl10A was statistically optimized for the hydrolysis of PCS glucan in the presence of Bgl3A. The resultant mixture achieved higher PCS glucan hydrolysis at lower enzyme loading than a culture filtrate from T. cellulolyticus or a commercial enzyme preparation, demonstrating that the five enzymes play a role as core enzymes in the hydrolysis of PCS glucan. In Conclusion: Core cellulolytic enzymes in the T. cellulolyticus cellulase system were identified to Cel5A, Cel6A, Cel7A, Xyl10A, and Bgl3A and characterized. The optimized mixture of these five enzymes was highly effective for the hydrolysis of PCS glucan, providing a foundation for future improvement of the T. cellulolyticus cellulase system.« less

Authors:
 [1];  [2];  [2];  [1];  [3]
+ Show Author Affiliations
  1. National Inst. of Advanced Industrial Science and Technology (AIST), Hiroshima (Japan)
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  3. Kyoto Univ. (Japan). Graduate School of Agriculture Division of Applied Biosciences
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO)
OSTI Identifier:
1164092
Report Number(s):
NREL/JA-2700-62636
Journal ID: ISSN 1754-6834; MainId:21814;UUID:c555315d-a327-e411-b769-d89d67132a6d;MainAdminID:10290
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; Talaromyces cellulolyticus; lignocellulose; cellulases; pretreated corn stover; enzymatic hydrolysis

Citation Formats

Inoue, Hiroyuki, Decker, Stephen R., Taylor, Larry E., Yano, Shinichi, and Sawayama, Shigeki. Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass. United States: N. p., 2014. Web. doi:10.1186/s13068-014-0151-5.
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Inoue, Hiroyuki, Decker, Stephen R., Taylor, Larry E., Yano, Shinichi, & Sawayama, Shigeki. Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass. United States. https://doi.org/10.1186/s13068-014-0151-5
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Inoue, Hiroyuki, Decker, Stephen R., Taylor, Larry E., Yano, Shinichi, and Sawayama, Shigeki. Thu . "Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass". United States. https://doi.org/10.1186/s13068-014-0151-5. https://www.osti.gov/servlets/purl/1164092.
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@article{osti_1164092,
title = {Identification and characterization of core cellulolytic enzymes from Talaromyces cellulolyticus (formerly Acremonium cellulolyticus) critical for hydrolysis of lignocellulosic biomass},
author = {Inoue, Hiroyuki and Decker, Stephen R. and Taylor, Larry E. and Yano, Shinichi and Sawayama, Shigeki},
abstractNote = {Background: Enzymatic hydrolysis of pretreated lignocellulosic biomass is an essential process for the production of fermentable sugars for industrial use. A better understanding of fungal cellulase systems will provide clues for maximizing the hydrolysis of target biomass. Talaromyces cellulolyticus is a promising fungus for cellulase production and efficient biomass hydrolysis. Several cellulolytic enzymes purified from T. cellulolyticus were characterized in earlier studies, but the core enzymes critical for hydrolysis of lignocellulosic biomass remain unknown. Results: Six cellulolytic enzymes critical for the hydrolysis of crystalline cellulose were purified from T. cellulolyticus culture supernatant using an enzyme assay based on synergistic hydrolysis of Avicel. The purified enzymes were identified by their substrate specificities and analyses of trypsin-digested peptide fragments and were classified into the following glycosyl hydrolase (GH) families: GH3 (β-glucosidase, Bgl3A), GH5 (endoglucanase, Cel5A), GH6 (cellobiohydrolase II, Cel6A), GH7 (cellobiohydrolase I and endoglucanase, Cel7A and Cel7B, respectively), and GH10 (xylanase, Xyl10A). Hydrolysis of dilute acid-pretreated corn stover (PCS) with mixtures of the purified enzymes showed that Cel5A, Cel7B, and Xyl10A each had synergistic effects with a mixture of Cel6A and Cel7A. Cel5A seemed to be more effective in the synergistic hydrolysis of the PCS than Cel7B. The ratio of Cel5A, Cel6A, Cel7A, and Xyl10A was statistically optimized for the hydrolysis of PCS glucan in the presence of Bgl3A. The resultant mixture achieved higher PCS glucan hydrolysis at lower enzyme loading than a culture filtrate from T. cellulolyticus or a commercial enzyme preparation, demonstrating that the five enzymes play a role as core enzymes in the hydrolysis of PCS glucan. In Conclusion: Core cellulolytic enzymes in the T. cellulolyticus cellulase system were identified to Cel5A, Cel6A, Cel7A, Xyl10A, and Bgl3A and characterized. The optimized mixture of these five enzymes was highly effective for the hydrolysis of PCS glucan, providing a foundation for future improvement of the T. cellulolyticus cellulase system.},
doi = {10.1186/s13068-014-0151-5},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 7,
place = {United States},
year = {Thu Oct 09 00:00:00 EDT 2014},
month = {Thu Oct 09 00:00:00 EDT 2014}
}
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https://doi.org/10.1186/s13068-014-0151-5
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Synthetic multi-component enzyme mixtures for deconstruction of lignocellulosic biomass
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journal, March 2009

Rapid optimization of enzyme mixtures for deconstruction of diverse pretreatment/biomass feedstock combinations
journal, January 2010

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Optimization of a synthetic mixture composed of major Trichoderma reesei enzymes for the hydrolysis of steam-exploded wheat straw
journal, January 2012

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  • Biotechnology for Biofuels, Vol. 5, Issue 1
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Purification and properties of thermostable xylanases from mesophilic fungus strain Y-94.
journal, January 1987

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  • Agricultural and Biological Chemistry, Vol. 51, Issue 12
  • DOI: 10.1271/bbb1961.51.3207

Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design
journal, September 2012

Purification and Some Properties of a Low Endo-type Cellulase from Acremonium cellulolyticus.
journal, January 2003

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Cellulase digestibility of pretreated biomass is limited by cellulose accessibility
journal, January 2007

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Alternatives to Trichoderma reesei in biofuel production
journal, September 2011

Construction of a starch-inducible homologous expression system to produce cellulolytic enzymes from Acremonium cellulolyticus
journal, May 2013

  • Inoue, Hiroyuki; Fujii, Tatsuya; Yoshimi, Miho
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Development of highly efficient, low-cost lignocellulolytic enzyme systems in the post-genomic era
journal, November 2013

Enzymatic hydrolyzing performance of Acremonium cellulolyticus and Trichoderma reesei against three lignocellulosic materials
journal, January 2009

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Synergistic enhancement of cellobiohydrolase performance on pretreated corn stover by addition of xylanase and esterase activities
journal, July 2008

Purification and Properties of a β-Glucosidase from Fungal Strain Y-94
journal, December 1989

Biomass pretreatment: Fundamentals toward application
journal, November 2011

Synthetic enzyme mixtures for biomass deconstruction: Production and optimization of a core set
journal, March 2010

  • Banerjee, Goutami; Car, Suzana; Scott-Craig, John S.
  • Biotechnology and Bioengineering, Vol. 106, Issue 5
  • DOI: 10.1002/bit.22741

Effect of xylan and lignin removal by batch and flowthrough pretreatment on the enzymatic digestibility of corn stover cellulose
journal, January 2004

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Taxonomic revision of the cellulose-degrading fungus Acremonium cellulolyticus nomen nudum to Talaromyces based on phylogenetic analysis
journal, December 2013

  • Fujii, Tatsuya; Hoshino, Tamotsu; Inoue, Hiroyuki
  • FEMS Microbiology Letters, Vol. 351, Issue 1
  • DOI: 10.1111/1574-6968.12352

High-coverage gene expression profiling analysis of the cellulase-producing fungus Acremonium cellulolyticus cultured using different carbon sources
journal, January 2013

  • Hideno, Akihiro; Inoue, Hiroyuki; Fujii, Tatsuya
  • Applied Microbiology and Biotechnology, Vol. 97, Issue 12
  • DOI: 10.1007/s00253-013-4689-0

Effects of Tween 80 on cellulase stability under agitated conditions
journal, August 2013

Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei
journal, May 2009

  • Nagendran, Subashini; Hallen-Adams, Heather E.; Paper, Janet M.
  • Fungal Genetics and Biology, Vol. 46, Issue 5
  • DOI: 10.1016/j.fgb.2009.02.001

Isolation of a Cellulolytic Enzyme Producing Microorganism, Culture Conditions and Some Properties of the Enzymes
journal, January 1987

  • Yamanobe, Takashi; Mitsuishi, Yasushi; Takasaki, Yoshiyuki
  • Agricultural and Biological Chemistry, Vol. 51, Issue 1
  • DOI: 10.1080/00021369.1987.10867998

Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview
journal, April 2002

Optimization of enzyme complexes for lignocellulose hydrolysis
journal, January 2007

  • Berlin, Alex; Maximenko, Vera; Gilkes, Neil
  • Biotechnology and Bioengineering, Vol. 97, Issue 2, p. 287-296
  • DOI: 10.1002/bit.21238

Pretreatment of Lignocellulosic Materials for Efficient Bioethanol Production
book, January 2007

Hemicellulases and auxiliary enzymes for improved conversion of lignocellulosic biomass to monosaccharides
journal, January 2011

  • Gao, Dahai; Uppugundla, Nirmal; Chundawat, Shishir PS
  • Biotechnology for Biofuels, Vol. 4, Issue 1
  • DOI: 10.1186/1754-6834-4-5

Effects of Tween 80 on cellulase stability under agitated conditions
journal, August 2013

Liquefaction of hydrothermally pretreated wheat straw at high-solids content by purified Trichoderma enzymes
journal, January 2011

Comparative performance of precommercial cellulases hydrolyzing pretreated corn stover
journal, January 2011

  • McMillan, James D.; Jennings, Edward W.; Mohagheghi, Ali
  • Biotechnology for Biofuels, Vol. 4, Issue 1
  • DOI: 10.1186/1754-6834-4-29

Purification and Properties of Thermostable Xylanases from Mesophilic Fungus Strain Y-94
journal, December 1987

  • Mitsuishi, Yasushi; Yamanobe, Takashi; Yagisawa, Mitsuo
  • Agricultural and Biological Chemistry, Vol. 51, Issue 12
  • DOI: 10.1080/00021369.1987.10868555

Biomass pretreatment: Fundamentals toward application
journal, November 2011

Synergistic enhancement of cellobiohydrolase performance on pretreated corn stover by addition of xylanase and esterase activities
journal, July 2008

Enzymatic hydrolyzing performance of Acremonium cellulolyticus and Trichoderma reesei against three lignocellulosic materials
journal, January 2009

  • Fujii, Tatsuya; Fang, Xu; Inoue, Hiroyuki
  • Biotechnology for Biofuels, Vol. 2, Issue 1
  • DOI: 10.1186/1754-6834-2-24

Xylanase (GH11) from Acremonium cellulolyticus: homologous expression and characterization
journal, April 2014

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
  • DOI: 10.1093/nar/gkn663

Evaluation of fluorescence-based thermal shift assays for hit identification in drug discovery
journal, September 2004

Evaluation of Minimal Trichoderma reesei Cellulase Mixtures on Differently Pretreated Barley Straw Substrates
journal, December 2007

  • Rosgaard, L.; Pedersen, S.; Langston, J.
  • Biotechnology Progress, Vol. 23, Issue 6
  • DOI: 10.1021/bp070329p
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    • Vijayaraghavan, Ponnuswamy; Arun, Arumugaperumal; Al-Dhabi, Naif Abdullah
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0481-6

    Genome sequencing and analysis of Talaromyces pinophilus provide insights into biotechnological applications
    journal, March 2017

    Engineering Robust Cellulases for Tailored Lignocellulosic Degradation Cocktails
    journal, February 2020

    • Contreras, Francisca; Pramanik, Subrata; M. Rozhkova, Aleksandra
    • International Journal of Molecular Sciences, Vol. 21, Issue 5
    • DOI: 10.3390/ijms21051589

    Comparative insights into the saccharification potentials of a relatively unexplored but robust Penicillium funiculosum glycoside hydrolase 7 cellobiohydrolase
    journal, March 2017

    • Ogunmolu, Funso Emmanuel; Jagadeesha, Navya Bhatt Kammachi; Kumar, Rakesh
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0752-x

    Engineering Robust Cellulases for Tailored Lignocellulosic Degradation Cocktails
    journal, February 2020

    • Contreras, Francisca; Pramanik, Subrata; M. Rozhkova, Aleksandra
    • International Journal of Molecular Sciences, Vol. 21, Issue 5
    • DOI: 10.3390/ijms21051589

    Characterization of cellulolytic enzyme system of Schizophyllum commune mutant and evaluation of its efficiency on biomass hydrolysis
    journal, May 2017

    • Sornlake, Warasirin; Rattanaphanjak, Phatcharamon; Champreda, Verawat
    • Bioscience, Biotechnology, and Biochemistry, Vol. 81, Issue 7
    • DOI: 10.1080/09168451.2017.1320937

    Engineering robust cellulases for tailored lignocellulosic degradation cocktails
    other, January 2020

    • Contreras, Francisca; Pramanik, Subrata; Rozhkova, Aleksandra M.
    • Basel : MDPI AG
    • DOI: 10.34657/5506

    Draft Genome Sequence of Talaromyces cellulolyticus Strain Y-94, a Source of Lignocellulosic Biomass-Degrading Enzymes
    journal, February 2015

    Mode of Action of GH30-7 Reducing-End Xylose-Releasing Exoxylanase A (Xyn30A) from the Filamentous Fungus Talaromyces cellulolyticus
    journal, April 2019

    • Nakamichi, Yusuke; Fouquet, Thierry; Ito, Shotaro
    • Applied and Environmental Microbiology, Vol. 85, Issue 13
    • DOI: 10.1128/aem.00552-19

    Biochemical characterization and synergism of cellulolytic enzyme system from Chaetomium globosum on rice straw saccharification
    journal, November 2016

    • Wanmolee, Wanwitoo; Sornlake, Warasirin; Rattanaphan, Nakul
    • BMC Biotechnology, Vol. 16, Issue 1
    • DOI: 10.1186/s12896-016-0312-7

    Draft Genome Sequence of Talaromyces cellulolyticus Strain Y-94, a Source of Lignocellulosic Biomass-Degrading Enzymes
    journal, February 2015

    Engineering Robust Cellulases for Tailored Lignocellulosic Degradation Cocktails
    text, January 2020

    Talaromyces borbonicus , sp. nov., a novel fungus from biodegraded Arundo donax with potential abilities in lignocellulose conversion
    journal, March 2018

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