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Title: Biochemical and structural characterizations of two Dictyostelium cellobiohydrolases from the amoebozoa kingdom reveal a high level of conservation between distant phylogenetic trees of life

Abstract

Glycoside hydrolase family 7 (GH7) cellobiohydrolases (CBHs) are enzymes often employed in plant cell wall degradation across eukaryotic kingdoms of life, as they provide significant hydrolytic potential in cellulose turnover. To date, many fungal GH7 CBHs have been examined, yet many questions regarding structure-activity relationships in these important natural and commercial enzymes remain. Here, we present the crystal structures and a biochemical analysis of two GH7 CBHs from social amoeba: Dictyostelium discoideum Cel7A (DdiCel7A) and Dictyostelium purpureum Cel7A (DpuCel7A). DdiCel7A and DpuCel7A natively consist of a catalytic domain and do not exhibit a carbohydrate-binding module (CBM). The structures of DdiCel7A and DpuCel7A, resolved to 2.1 Å and 2.7 Å, respectively, are homologous to those of other GH7 CBHs with an enclosed active-site tunnel. Two primary differences between the Dictyostelium CBHs and the archetypal model GH7 CBH, Trichoderma reesei Cel7A (TreCel7A), occur near the hydrolytic active site and the product-binding sites. To compare the activities of these enzymes with the activity of TreCel7A, the family 1 TreCel7A CBM and linker were added to the C terminus of each of the Dictyostelium enzymes, creating DdiCel7ACBM and DpuCel7ACBM, which were recombinantly expressed in T. reesei. DdiCel7ACBM and DpuCel7ACBM hydrolyzed Avicel, pretreated corn stover,more » and phosphoric acid-swollen cellulose as efficiently as TreCel7A when hydrolysis was compared at their temperature optima. The Ki of cellobiose was significantly higher for DdiCel7ACBM and DpuCel7ACBM than for TreCel7A: 205, 130, and 29 μM, respectively. Finally, taken together, the present study highlights the remarkable degree of conservation of the activity of these key natural and industrial enzymes across quite distant phylogenetic trees of life.« less

Authors:
 [1];  [2];  [3];  [1];  [3];  [1];  [1];  [1];  [1];  [2];  [3]
+ Show Author Affiliations
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States). National Bioenergy Center
  3. Swedish Univ. of Agricultural Sciences, Uppsala, (Sweden). Dept. of Chemistry and Biotechnology
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office
OSTI Identifier:
1257747
Report Number(s):
NREL/JA-5100-66281
Journal ID: ISSN 0099-2240
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 82; Journal Issue: 11; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; enzymes; plant cell wall degradation; hydrolytic potential

Citation Formats

Hobdey, Sarah E., Knott, Brandon C., Momeni, Majid Haddad, Taylor, II, Larry E., Borisova, Anna S., Podkaminer, Kara K., VanderWall, Todd A., Himmel, Michael E., Decker, Stephen R., Beckham, Gregg T., and Stahlberg, Jerry. Biochemical and structural characterizations of two Dictyostelium cellobiohydrolases from the amoebozoa kingdom reveal a high level of conservation between distant phylogenetic trees of life. United States: N. p., 2016. Web. doi:10.1128/AEM.00163-16.
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Hobdey, Sarah E., Knott, Brandon C., Momeni, Majid Haddad, Taylor, II, Larry E., Borisova, Anna S., Podkaminer, Kara K., VanderWall, Todd A., Himmel, Michael E., Decker, Stephen R., Beckham, Gregg T., & Stahlberg, Jerry. Biochemical and structural characterizations of two Dictyostelium cellobiohydrolases from the amoebozoa kingdom reveal a high level of conservation between distant phylogenetic trees of life. United States. https://doi.org/10.1128/AEM.00163-16
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Hobdey, Sarah E., Knott, Brandon C., Momeni, Majid Haddad, Taylor, II, Larry E., Borisova, Anna S., Podkaminer, Kara K., VanderWall, Todd A., Himmel, Michael E., Decker, Stephen R., Beckham, Gregg T., and Stahlberg, Jerry. Fri . "Biochemical and structural characterizations of two Dictyostelium cellobiohydrolases from the amoebozoa kingdom reveal a high level of conservation between distant phylogenetic trees of life". United States. https://doi.org/10.1128/AEM.00163-16. https://www.osti.gov/servlets/purl/1257747.
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@article{osti_1257747,
title = {Biochemical and structural characterizations of two Dictyostelium cellobiohydrolases from the amoebozoa kingdom reveal a high level of conservation between distant phylogenetic trees of life},
author = {Hobdey, Sarah E. and Knott, Brandon C. and Momeni, Majid Haddad and Taylor, II, Larry E. and Borisova, Anna S. and Podkaminer, Kara K. and VanderWall, Todd A. and Himmel, Michael E. and Decker, Stephen R. and Beckham, Gregg T. and Stahlberg, Jerry},
abstractNote = {Glycoside hydrolase family 7 (GH7) cellobiohydrolases (CBHs) are enzymes often employed in plant cell wall degradation across eukaryotic kingdoms of life, as they provide significant hydrolytic potential in cellulose turnover. To date, many fungal GH7 CBHs have been examined, yet many questions regarding structure-activity relationships in these important natural and commercial enzymes remain. Here, we present the crystal structures and a biochemical analysis of two GH7 CBHs from social amoeba: Dictyostelium discoideum Cel7A (DdiCel7A) and Dictyostelium purpureum Cel7A (DpuCel7A). DdiCel7A and DpuCel7A natively consist of a catalytic domain and do not exhibit a carbohydrate-binding module (CBM). The structures of DdiCel7A and DpuCel7A, resolved to 2.1 Å and 2.7 Å, respectively, are homologous to those of other GH7 CBHs with an enclosed active-site tunnel. Two primary differences between the Dictyostelium CBHs and the archetypal model GH7 CBH, Trichoderma reesei Cel7A (TreCel7A), occur near the hydrolytic active site and the product-binding sites. To compare the activities of these enzymes with the activity of TreCel7A, the family 1 TreCel7A CBM and linker were added to the C terminus of each of the Dictyostelium enzymes, creating DdiCel7ACBM and DpuCel7ACBM, which were recombinantly expressed in T. reesei. DdiCel7ACBM and DpuCel7ACBM hydrolyzed Avicel, pretreated corn stover, and phosphoric acid-swollen cellulose as efficiently as TreCel7A when hydrolysis was compared at their temperature optima. The Ki of cellobiose was significantly higher for DdiCel7ACBM and DpuCel7ACBM than for TreCel7A: 205, 130, and 29 μM, respectively. Finally, taken together, the present study highlights the remarkable degree of conservation of the activity of these key natural and industrial enzymes across quite distant phylogenetic trees of life.},
doi = {10.1128/AEM.00163-16},
journal = {Applied and Environmental Microbiology},
number = 11,
volume = 82,
place = {United States},
year = {Fri Apr 01 00:00:00 EDT 2016},
month = {Fri Apr 01 00:00:00 EDT 2016}
}
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https://doi.org/10.1128/AEM.00163-16
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