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Title: Tracking of enzymatic biomass deconstruction by fungal secretomes highlights markers of lignocellulose recalcitrance

Abstract

Background:Lignocellulose biomass is known as a recalcitrant material towards enzymatic hydrolysis, increasing the process cost in biorefinery. In nature, filamentous fungi naturally degrade lignocellulose, using an arsenal of hydrolytic and oxidative enzymes. Assessment of enzyme hydrolysis efficiency generally relies on the yield of glucose for a given biomass. To better understand the markers governing recalcitrance to enzymatic degradation, there is a need to enlarge the set of parameters followed during deconstruction. Results:Industrially-pretreated biomass feedstocks from wheat straw, miscanthus and poplar were sequentially hydrolysed following two steps. First, standard secretome from Trichoderma reesei was used to maximize cellulose hydrolysis, producing three recalcitrant lignin-enriched solid substrates. Then fungal secretomes from three basidiomycete saprotrophs ( Laetisaria arvalis, Artolenzites elegans and Trametes ljubarskyi) displaying various hydrolytic and oxidative enzymatic profiles were applied to these recalcitrant substrates, and compared to the T. reesei secretome. As a result, most of the glucose was released after the first hydrolysis step. After the second hydrolysis step, half of the remaining glucose amount was released. Overall, glucose yield after the two sequential hydrolyses was more dependent on the biomass source than on the fungal secretomes enzymatic profile. Solid residues obtained after the two hydrolysis steps were characterized using complementary methodologies.more » Correlation analysis of several physico-chemical parameters showed that released glucose yield was negatively correlated with lignin content and cellulose crystallinity while positively correlated with xylose content and water sorption. Water sorption appears as a pivotal marker of the recalcitrance as it reflects chemical and structural properties of lignocellulosic biomass. Conclusions:Fungal secretomes applied to highly recalcitrant biomass samples can further extend the release of the remaining glucose. The glucose yield can be correlated to chemical and physical markers, which appear to be independent from the biomass type and secretome. Overall, correlations between these markers reveal how nano-scale properties (polymer content and organization) influence macro-scale properties (particle size and water sorption). Further systematic assessment of these markers during enzymatic degradation will foster the development of novel cocktails to unlock the degradation of lignocellulose biomass.« less

Authors:
 [1];  [2];  [3];  [3];  [1];  [3];  [4];  [5];  [6];  [2];  [7];  [5];  [3];  [7];  [2];  [2];  [5]; ORCiD logo [2]
  1. Univ. de Reims Champagne-Ardenne, Reims (France). l’Inst. National de Recherche Agronomique (INRA), FARE Lab.
  2. Aix-Marseille Univ., Marseille (France)
  3. IFP Energies Nouvelles, Rueil-Malmaison (France)
  4. Aix-Marseille Univ., and CNRS, Marseille (France)
  5. l’Inst. National de Recherche Agronomique (INRA), Nantes (France)
  6. Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Univ. Grenoble Alpes, Grenoble (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1560574
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Paës, Gabriel, Navarro, David, Benoit, Yves, Blanquet, Senta, Chabbert, Brigitte, Chaussepied, Bernard, Coutinho, Pedro M., Durand, Sylvie, Grigoriev, Igor V., Haon, Mireille, Heux, Laurent, Launay, Charlène, Margeot, Antoine, Nishiyama, Yoshiharu, Raouche, Sana, Rosso, Marie-Noëlle, Bonnin, Estelle, and Berrin, Jean-Guy. Tracking of enzymatic biomass deconstruction by fungal secretomes highlights markers of lignocellulose recalcitrance. United States: N. p., 2019. Web. doi:10.1186/s13068-019-1417-8.
Paës, Gabriel, Navarro, David, Benoit, Yves, Blanquet, Senta, Chabbert, Brigitte, Chaussepied, Bernard, Coutinho, Pedro M., Durand, Sylvie, Grigoriev, Igor V., Haon, Mireille, Heux, Laurent, Launay, Charlène, Margeot, Antoine, Nishiyama, Yoshiharu, Raouche, Sana, Rosso, Marie-Noëlle, Bonnin, Estelle, & Berrin, Jean-Guy. Tracking of enzymatic biomass deconstruction by fungal secretomes highlights markers of lignocellulose recalcitrance. United States. doi:10.1186/s13068-019-1417-8.
Paës, Gabriel, Navarro, David, Benoit, Yves, Blanquet, Senta, Chabbert, Brigitte, Chaussepied, Bernard, Coutinho, Pedro M., Durand, Sylvie, Grigoriev, Igor V., Haon, Mireille, Heux, Laurent, Launay, Charlène, Margeot, Antoine, Nishiyama, Yoshiharu, Raouche, Sana, Rosso, Marie-Noëlle, Bonnin, Estelle, and Berrin, Jean-Guy. Mon . "Tracking of enzymatic biomass deconstruction by fungal secretomes highlights markers of lignocellulose recalcitrance". United States. doi:10.1186/s13068-019-1417-8. https://www.osti.gov/servlets/purl/1560574.
@article{osti_1560574,
title = {Tracking of enzymatic biomass deconstruction by fungal secretomes highlights markers of lignocellulose recalcitrance},
author = {Paës, Gabriel and Navarro, David and Benoit, Yves and Blanquet, Senta and Chabbert, Brigitte and Chaussepied, Bernard and Coutinho, Pedro M. and Durand, Sylvie and Grigoriev, Igor V. and Haon, Mireille and Heux, Laurent and Launay, Charlène and Margeot, Antoine and Nishiyama, Yoshiharu and Raouche, Sana and Rosso, Marie-Noëlle and Bonnin, Estelle and Berrin, Jean-Guy},
abstractNote = {Background:Lignocellulose biomass is known as a recalcitrant material towards enzymatic hydrolysis, increasing the process cost in biorefinery. In nature, filamentous fungi naturally degrade lignocellulose, using an arsenal of hydrolytic and oxidative enzymes. Assessment of enzyme hydrolysis efficiency generally relies on the yield of glucose for a given biomass. To better understand the markers governing recalcitrance to enzymatic degradation, there is a need to enlarge the set of parameters followed during deconstruction. Results:Industrially-pretreated biomass feedstocks from wheat straw, miscanthus and poplar were sequentially hydrolysed following two steps. First, standard secretome from Trichoderma reesei was used to maximize cellulose hydrolysis, producing three recalcitrant lignin-enriched solid substrates. Then fungal secretomes from three basidiomycete saprotrophs (Laetisaria arvalis, Artolenzites elegans and Trametes ljubarskyi) displaying various hydrolytic and oxidative enzymatic profiles were applied to these recalcitrant substrates, and compared to the T. reesei secretome. As a result, most of the glucose was released after the first hydrolysis step. After the second hydrolysis step, half of the remaining glucose amount was released. Overall, glucose yield after the two sequential hydrolyses was more dependent on the biomass source than on the fungal secretomes enzymatic profile. Solid residues obtained after the two hydrolysis steps were characterized using complementary methodologies. Correlation analysis of several physico-chemical parameters showed that released glucose yield was negatively correlated with lignin content and cellulose crystallinity while positively correlated with xylose content and water sorption. Water sorption appears as a pivotal marker of the recalcitrance as it reflects chemical and structural properties of lignocellulosic biomass. Conclusions:Fungal secretomes applied to highly recalcitrant biomass samples can further extend the release of the remaining glucose. The glucose yield can be correlated to chemical and physical markers, which appear to be independent from the biomass type and secretome. Overall, correlations between these markers reveal how nano-scale properties (polymer content and organization) influence macro-scale properties (particle size and water sorption). Further systematic assessment of these markers during enzymatic degradation will foster the development of novel cocktails to unlock the degradation of lignocellulose biomass.},
doi = {10.1186/s13068-019-1417-8},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 12,
place = {United States},
year = {2019},
month = {4}
}

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Free Publicly Available Full Text
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Cited by: 4 works
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Figures / Tables:

Fig. 1 Fig. 1: Biomass pre‑treatment and sequential hydrolysis steps by fungal enzymatic secretomes of the biomass materials (poplar, wheat straw and miscanthus). R and S indicate residual (solid) and soluble fractions, respectively

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The role of pretreatment in improving the enzymatic hydrolysis of lignocellulosic materials
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    Works referencing / citing this record:

    Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina)
    journal, May 2008

    • Martinez, Diego; Berka, Randy M.; Henrissat, Bernard
    • Nature Biotechnology, Vol. 26, Issue 5
    • DOI: 10.1038/nbt1403

    Heterogeneity in the chemistry, structure and function of plant cell walls
    journal, September 2010

    • Burton, Rachel A.; Gidley, Michael J.; Fincher, Geoffrey B.
    • Nature Chemical Biology, Vol. 6, Issue 10
    • DOI: 10.1038/nchembio.439

    Cellulase adsorption on lignin: A roadblock for economic hydrolysis of biomass
    journal, December 2016


    The grand challenge of cellulosic biofuels
    journal, October 2017


    Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer
    journal, December 2015

    • Westereng, Bjørge; Cannella, David; Wittrup Agger, Jane
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep18561

    Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies
    journal, September 2009


    MycoCosm portal: gearing up for 1000 fungal genomes
    journal, December 2013

    • Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
    • Nucleic Acids Research, Vol. 42, Issue D1
    • DOI: 10.1093/nar/gkt1183

    How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility?
    journal, November 2012


    Fungal secretomics to probe the biological functions of lytic polysaccharide monooxygenases
    journal, August 2017


    Recent advances in understanding the role of cellulose accessibility in enzymatic hydrolysis of lignocellulosic substrates
    journal, June 2014


    Fast solubilization of recalcitrant cellulosic biomass by the basidiomycete fungus Laetisaria arvalisinvolves successive secretion of oxidative and hydrolytic enzymes
    journal, October 2014

    • Navarro, David; Rosso, Marie-Noëlle; Haon, Mireille
    • Biotechnology for Biofuels, Vol. 7, Issue 1
    • DOI: 10.1186/s13068-014-0143-5

    Lignocellulosic ethanol: From science to industry
    journal, November 2012


    A new stoichiometric miniaturization strategy for screening of industrial microbial strains: application to cellulase hyper-producing Trichoderma reesei strains
    journal, January 2012

    • Jourdier, Etienne; Poughon, Laurent; Larroche, Christian
    • Microbial Cell Factories, Vol. 11, Issue 1
    • DOI: 10.1186/1475-2859-11-70

    Rapid acid hydrolysis of plant cell wall polysaccharides and simplified quantitative determination of their neutral monosaccharides by gas-liquid chromatography
    journal, March 1989

    • Hoebler, Christine; Barry, Jean Luc; David, Agnes
    • Journal of Agricultural and Food Chemistry, Vol. 37, Issue 2
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    Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
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    • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
    • Science, Vol. 315, Issue 5813, p. 804-807
    • DOI: 10.1126/science.1137016

    Biomass recalcitrance. Part I: the chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose
    journal, March 2012

    • Zhao, Xuebing; Zhang, Lihua; Liu, Dehua
    • Biofuels, Bioproducts and Biorefining, Vol. 6, Issue 4
    • DOI: 10.1002/bbb.1331

    Multiscale deconstruction of molecular architecture in corn stover
    journal, January 2014

    • Inouye, Hideyo; Zhang, Yan; Yang, Lin
    • Scientific Reports, Vol. 4, Issue 1
    • DOI: 10.1038/srep03756

    Action of lytic polysaccharide monooxygenase on plant tissue is governed by cellular type
    journal, December 2017


    Effects of grinding processes on enzymatic degradation of wheat straw
    journal, January 2012


    New improvements for lignocellulosic ethanol
    journal, June 2009

    • Margeot, Antoine; Hahn-Hagerdal, Bärbel; Edlund, Maria
    • Current Opinion in Biotechnology, Vol. 20, Issue 3
    • DOI: 10.1016/j.copbio.2009.05.009

    Multimodal analysis of pretreated biomass species highlights generic markers of lignocellulose recalcitrance
    journal, February 2018

    • Herbaut, Mickaël; Zoghlami, Aya; Habrant, Anouck
    • Biotechnology for Biofuels, Vol. 11, Issue 1
    • DOI: 10.1186/s13068-018-1053-8

    Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina
    journal, June 2015

    • Bennati-Granier, Chloé; Garajova, Sona; Champion, Charlotte
    • Biotechnology for Biofuels, Vol. 8, Issue 1
    • DOI: 10.1186/s13068-015-0274-3

    Fungal Enzymes for Bio-Products from Sustainable and Waste Biomass
    journal, July 2016

    • Gupta, Vijai K.; Kubicek, Christian P.; Berrin, Jean-Guy
    • Trends in Biochemical Sciences, Vol. 41, Issue 7
    • DOI: 10.1016/j.tibs.2016.04.006

    Fungal Cellulases
    journal, January 2015

    • Payne, Christina M.; Knott, Brandon C.; Mayes, Heather B.
    • Chemical Reviews, Vol. 115, Issue 3
    • DOI: 10.1021/cr500351c

    Xylans inhibit enzymatic hydrolysis of lignocellulosic materials by cellulases
    journal, October 2012


    Water sorption in pretreated grasses as a predictor of enzymatic hydrolysis yields
    journal, December 2017


    Current Pretreatment Technologies for the Development of Cellulosic Ethanol and Biorefineries
    journal, September 2015

    • Silveira, Marcos Henrique Luciano; Morais, Ana Rita C.; da Costa Lopes, Andre M.
    • ChemSusChem, Vol. 8, Issue 20
    • DOI: 10.1002/cssc.201500282

    FunGene-DB: A web-based tool for Polyporales strains authentication
    journal, October 2012


    Testing scientific models using Qualitative Reasoning: Application to cellulose hydrolysis
    journal, October 2017


    Undefined cellulase formulations hinder scientific reproducibility
    journal, November 2017

    • Himmel, Michael E.; Abbas, Charles A.; Baker, John O.
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0974-y

    Understanding the structural and chemical changes of plant biomass following steam explosion pretreatment
    journal, February 2017

    • Auxenfans, Thomas; Crônier, David; Chabbert, Brigitte
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0718-z

    Cellulosic Biomass Pretreatment and Sugar Yields as a Function of Biomass Particle Size
    journal, June 2014


    Steam explosion pretreatment of softwood: the effect of the explosive decompression on enzymatic digestibility
    journal, July 2016

    • Pielhop, Thomas; Amgarten, Janick; von Rohr, Philipp Rudolf
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0567-1

    Production and applications of carbohydrate-derived sugar acids as generic biobased chemicals
    journal, July 2015


    Lignin-enzyme interaction: Mechanism, mitigation approach, modeling, and research prospects
    journal, July 2017


    Plant cell wall polymers as precursors for biofuels
    journal, June 2010


    Hydrothermal pretreatment of wood by mild steam explosion and hot water extraction
    journal, October 2017


    A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis
    journal, November 2017

    • Escamez, Sacha; Latha Gandla, Madhavi; Derba-Maceluch, Marta
    • Scientific Reports, Vol. 7, Issue 1
    • DOI: 10.1038/s41598-017-16013-0

    Impact of lignin on water sorption properties of bioinspired self-assemblies of lignocellulosic polymers
    journal, March 2015


    Database resources of the National Center for Biotechnology Information
    journal, November 2017

    • Agarwala, Richa; Barrett, Tanya; Beck, Jeff
    • Nucleic Acids Research, Vol. 46, Issue D1
    • DOI: 10.1093/nar/gkx1095

    The role of pretreatment in improving the enzymatic hydrolysis of lignocellulosic materials
    journal, January 2016


    Current Understanding of the Correlation of Lignin Structure with Biomass Recalcitrance
    journal, November 2016


    Impact of delignification on the morphology and the reactivity of steam exploded wheat straw
    journal, January 2016


    Improved Saccharification of Wheat Straw for Biofuel Production Using an Engineered Secretome of Trichoderma reesei
    journal, January 2011

    • Ayrinhac, Céline; Margeot, Antoine; Ferreira, Nicolas Lopes
    • Organic Process Research & Development, Vol. 15, Issue 1
    • DOI: 10.1021/op100218a

    Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis
    journal, January 2012


    Dynamical assessment of fluorescent probes mobility in poplar cell walls reveals nanopores govern saccharification
    journal, October 2018

    • Herbaut, Mickaël; Zoghlami, Aya; Paës, Gabriel
    • Biotechnology for Biofuels, Vol. 11, Issue 1
    • DOI: 10.1186/s13068-018-1267-9

    OrthoDB v9.1: cataloging evolutionary and functional annotations for animal, fungal, plant, archaeal, bacterial and viral orthologs
    journal, November 2016

    • Zdobnov, Evgeny M.; Tegenfeldt, Fredrik; Kuznetsov, Dmitry
    • Nucleic Acids Research, Vol. 45, Issue D1
    • DOI: 10.1093/nar/gkw1119

    Determination of lignin in herbaceous plants by an improved acetyl bromide procedure
    journal, January 1990

    • Iiyama, Kenji; Wallis, Adrian F. A.
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    What cell wall components are the best indicators for Miscanthus digestibility and conversion to ethanol following variable pretreatments?
    journal, March 2018

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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.