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Title: Correlation of structure, function and protein dynamics in GH7 cellobiohydrolases from Trichoderma atroviride, T. reesei and T. harzianum

Abstract

The ascomycete fungus Trichoderma reesei is the predominant source of enzymes for industrial conversion of lignocellulose. Its glycoside hydrolase family 7 cellobiohydrolase (GH7 CBH) TreCel7A constitutes nearly half of the enzyme cocktail by weight and is the major workhorse in the cellulose hydrolysis process. The orthologs from Trichoderma atroviride (TatCel7A) and Trichoderma harzianum (ThaCel7A) show high sequence identity with TreCel7A, ~ 80%, and represent naturally evolved combinations of cellulose-binding tunnel-enclosing loop motifs, which have been suggested to influence intrinsic cellobiohydrolase properties, such as endo-initiation, processivity, and off-rate. The TatCel7A, ThaCel7A, and TreCel7A enzymes were characterized for comparison of function. The catalytic domain of TatCel7A was crystallized, and two structures were determined: without ligand and with thio-cellotriose in the active site. Initial hydrolysis of bacterial cellulose was faster with TatCel7A than either ThaCel7A or TreCel7A. In synergistic saccharification of pretreated corn stover, both TatCel7A and ThaCel7A were more efficient than TreCel7A, although TatCel7A was more sensitive to thermal inactivation. Structural analyses and molecular dynamics (MD) simulations were performed to elucidate important structure/function correlations. Moreover, reverse conservation analysis (RCA) of sequence diversity revealed divergent regions of interest located outside the cellulose-binding tunnel of Trichoderma spp. GH7 CBHs. We hypothesize that the combinationmore » of loop motifs is the main determinant for the observed differences in Cel7A activity on cellulosic substrates. Fine-tuning of the loop flexibility appears to be an important evolutionary target in Trichoderma spp., a conclusion supported by the RCA data. Our results indicate that, for industrial use, it would be beneficial to combine loop motifs from TatCel7A with the thermostability features of TreCel7A. Furthermore, one region implicated in thermal unfolding is suggested as a primary target for protein engineering.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [6];  [7];  [7];  [5];  [4];  [8];  [9]; ORCiD logo [7]
+ Show Author Affiliations
  1. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Molecular Sciences; National Research Centre "Kurchatov Inst.", Gatchina (Russian Federation). B.P. Konstantinov Petersburg Nuclear Physics Inst.
  2. National Research Centre "Kurchatov Inst.", Gatchina (Russian Federation). B.P. Konstantinov Petersburg Nuclear Physics Inst.
  3. Univ. of Kentucky, Lexington, KY (United States). Dept. of Chemical and Materials Engineering
  4. Roskilde Univ. (Denmark). Dept. of Science and Environment
  5. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
  6. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Forest Mycology and Plant Pathology
  7. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Molecular Sciences
  8. Univ. of Kentucky, Lexington, KY (United States). Dept. of Chemical and Materials Engineering; National Science Foundation, Alexandria, VA (United States). Division of Chemical, Bioengineering, Environmental, and Transport Systems
  9. National Research Centre "Kurchatov Inst.", Gatchina (Russian Federation). B.P. Konstantinov Petersburg Nuclear Physics Inst.; Peter the Great St. Petersburg Polytechnic Univ., St. Petersburg (Russian Federation). Dept. of Medical Physics
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); Swedish Univ. of Agricultural Sciences, Uppsala (Sweden); National Research Centre "Kurchatov Inst.", Gatchina (Russian Federation); Roskilde Univ. (Denmark)
Sponsoring Org.:
USDOE; National Science Foundation (NSF); Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Sweden); Russian Science Foundation (Russian Federation); Novo Nordisk Foundation (Denmark); Innovation Fund Denmark
OSTI Identifier:
1423554
Report Number(s):
NREL/JA-2700-71016
Journal ID: ISSN 1754-6834
Grant/Contract Number:  
AC36-08GO28308; 1552355; ACI-1548562; 213-2013-1607; 16-14-00109; NNF15OC0016606; 5150-00020B
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; cellobiohydrolase; Trichoderma atroviride; Trichoderma harzianum; Trichoderma reesei; cellulase engineering

Citation Formats

Borisova, Anna S., Eneyskaya, Elena V., Jana, Suvamay, Badino, Silke F., Kari, Jeppe, Amore, Antonella, Karlsson, Magnus, Hansson, Henrik, Sandgren, Mats, Himmel, Michael E., Westh, Peter, Payne, Christina M., Kulminskaya, Anna A., and Ståhlberg, Jerry. Correlation of structure, function and protein dynamics in GH7 cellobiohydrolases from Trichoderma atroviride, T. reesei and T. harzianum. United States: N. p., 2018. Web. doi:10.1186/s13068-017-1006-7.
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Borisova, Anna S., Eneyskaya, Elena V., Jana, Suvamay, Badino, Silke F., Kari, Jeppe, Amore, Antonella, Karlsson, Magnus, Hansson, Henrik, Sandgren, Mats, Himmel, Michael E., Westh, Peter, Payne, Christina M., Kulminskaya, Anna A., & Ståhlberg, Jerry. Correlation of structure, function and protein dynamics in GH7 cellobiohydrolases from Trichoderma atroviride, T. reesei and T. harzianum. United States. https://doi.org/10.1186/s13068-017-1006-7
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Borisova, Anna S., Eneyskaya, Elena V., Jana, Suvamay, Badino, Silke F., Kari, Jeppe, Amore, Antonella, Karlsson, Magnus, Hansson, Henrik, Sandgren, Mats, Himmel, Michael E., Westh, Peter, Payne, Christina M., Kulminskaya, Anna A., and Ståhlberg, Jerry. Sat . "Correlation of structure, function and protein dynamics in GH7 cellobiohydrolases from Trichoderma atroviride, T. reesei and T. harzianum". United States. https://doi.org/10.1186/s13068-017-1006-7. https://www.osti.gov/servlets/purl/1423554.
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@article{osti_1423554,
title = {Correlation of structure, function and protein dynamics in GH7 cellobiohydrolases from Trichoderma atroviride, T. reesei and T. harzianum},
author = {Borisova, Anna S. and Eneyskaya, Elena V. and Jana, Suvamay and Badino, Silke F. and Kari, Jeppe and Amore, Antonella and Karlsson, Magnus and Hansson, Henrik and Sandgren, Mats and Himmel, Michael E. and Westh, Peter and Payne, Christina M. and Kulminskaya, Anna A. and Ståhlberg, Jerry},
abstractNote = {The ascomycete fungus Trichoderma reesei is the predominant source of enzymes for industrial conversion of lignocellulose. Its glycoside hydrolase family 7 cellobiohydrolase (GH7 CBH) TreCel7A constitutes nearly half of the enzyme cocktail by weight and is the major workhorse in the cellulose hydrolysis process. The orthologs from Trichoderma atroviride (TatCel7A) and Trichoderma harzianum (ThaCel7A) show high sequence identity with TreCel7A, ~ 80%, and represent naturally evolved combinations of cellulose-binding tunnel-enclosing loop motifs, which have been suggested to influence intrinsic cellobiohydrolase properties, such as endo-initiation, processivity, and off-rate. The TatCel7A, ThaCel7A, and TreCel7A enzymes were characterized for comparison of function. The catalytic domain of TatCel7A was crystallized, and two structures were determined: without ligand and with thio-cellotriose in the active site. Initial hydrolysis of bacterial cellulose was faster with TatCel7A than either ThaCel7A or TreCel7A. In synergistic saccharification of pretreated corn stover, both TatCel7A and ThaCel7A were more efficient than TreCel7A, although TatCel7A was more sensitive to thermal inactivation. Structural analyses and molecular dynamics (MD) simulations were performed to elucidate important structure/function correlations. Moreover, reverse conservation analysis (RCA) of sequence diversity revealed divergent regions of interest located outside the cellulose-binding tunnel of Trichoderma spp. GH7 CBHs. We hypothesize that the combination of loop motifs is the main determinant for the observed differences in Cel7A activity on cellulosic substrates. Fine-tuning of the loop flexibility appears to be an important evolutionary target in Trichoderma spp., a conclusion supported by the RCA data. Our results indicate that, for industrial use, it would be beneficial to combine loop motifs from TatCel7A with the thermostability features of TreCel7A. Furthermore, one region implicated in thermal unfolding is suggested as a primary target for protein engineering.},
doi = {10.1186/s13068-017-1006-7},
journal = {Biotechnology for Biofuels},
number = ,
volume = 11,
place = {United States},
year = {Sat Jan 13 00:00:00 EST 2018},
month = {Sat Jan 13 00:00:00 EST 2018}
}
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    Aromatic residues surrounding the active site tunnel of TfCel48A influence activity, processivity, and synergistic interactions with other cellulases
    journal, July 2019

    • Hefferon, Kathleen L.; Cantero‐Tubilla, Borja; Brady, John
    • Biotechnology and Bioengineering, Vol. 116, Issue 10
    • DOI: 10.1002/bit.27086

    Gene Co-expression Network Reveals Potential New Genes Related to Sugarcane Bagasse Degradation in Trichoderma reesei RUT-30
    journal, October 2018

    • Borin, Gustavo Pagotto; Carazzolle, Marcelo Falsarella; dos Santos, Renato Augusto Corrêa
    • Frontiers in Bioengineering and Biotechnology, Vol. 6
    • DOI: 10.3389/fbioe.2018.00151

    Synthesis of Human Milk Oligosaccharides: Protein Engineering Strategies for Improved Enzymatic Transglycosylation
    journal, May 2019

    Structural and biochemical characterization of a family 7 highly thermostable endoglucanase from the fungus Rasamsonia emersonii
    journal, December 2019

    • Schiano‐di‐Cola, Corinna; Kołaczkowski, Bartłomiej; Sørensen, Trine Holst
    • The FEBS Journal, Vol. 287, Issue 12
    • DOI: 10.1111/febs.15151

    pH profiles of cellulases depend on the substrate and architecture of the binding region
    journal, November 2019

    • Røjel, Nanna; Kari, Jeppe; Sørensen, Trine H.
    • Biotechnology and Bioengineering, Vol. 117, Issue 2
    • DOI: 10.1002/bit.27206

    Ega3 from the fungal pathogen Aspergillus fumigatus is an endo-α-1,4-galactosaminidase that disrupts microbial biofilms
    journal, August 2019

    • Bamford, Natalie C.; Le Mauff, François; Subramanian, Adithya S.
    • Journal of Biological Chemistry, Vol. 294, Issue 37
    • DOI: 10.1074/jbc.ra119.009910

    Synthesis of Human Milk Oligosaccharides: Protein Engineering Strategies for Improved Enzymatic Transglycosylation
    journal, May 2019

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