Enzyme kinetics by GH7 cellobiohydrolases on chromogenic substrates is dictated by non‐productive binding: insights from crystal structures and MD simulation
Abstract
Cellobiohydrolases (CBHs) in the glycoside hydrolase family 7 (GH7) ( EC3.2.1.176 ) are the major cellulose degrading enzymes both in industrial settings and in the context of carbon cycling in nature. Small carbohydrate conjugates such as p‐ nitrophenyl‐β‐ d ‐cellobioside (pNPC), p‐ nitrophenyl‐β‐ d ‐lactoside (pNPL) and methylumbelliferyl‐β‐ d ‐cellobioside have commonly been used in colorimetric and fluorometric assays for analysing activity of these enzymes. Despite the similar nature of these compounds the kinetics of their enzymatic hydrolysis vary greatly between the different compounds as well as among different enzymes within the GH7 family. Through enzyme kinetics, crystallographic structure determination, molecular dynamics simulations, and fluorometric binding studies using the closely related compound o‐nitrophenyl‐β‐ d ‐cellobioside (oNPC), in this work we examine the different hydrolysis characteristics of these compounds on two model enzymes of this class, TrCel7A from Trichoderma reesei and PcCel7D from Phanerochaete chrysosporium . Protein crystal structures of the E212Q mutant of TrCel7A with pNPC and pNPL, and the wildtype TrCel7A with oNPC, reveal that non‐productive binding at the product site is the dominating binding mode for these compounds. Enzyme kinetics results suggest the strength of non‐productive binding is a key determinant for the activity characteristics on these substrates, with PcCel7Dmore »
- Authors:
-
- Department of Molecular Sciences Swedish University of Agricultural Sciences Uppsala Sweden
- Department of Chemical and Materials Engineering University of Kentucky Lexington KY USA, Renewable Resources and Enabling Sciences Center National Renewable Energy Laboratory Golden CO USA
- Department of Chemistry Uppsala University Sweden, Institute of Molecular and Cell Biology University of Tartu Estonia
- Department of Chemical and Materials Engineering University of Kentucky Lexington KY USA
- Institute of Chemistry and Biomedical Sciences Linnaeus University Kalmar Sweden
- Institute of Molecular and Cell Biology University of Tartu Estonia
- Department of Chemistry Uppsala University Sweden
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE); Swedish Research Council (SRC); Swedish Governmental Agency for Innovation Systems; Swedish Energy Agency; Swedish Natural Science Research Council (NFR); National Science Foundation (NSF); Estonian Research Council
- OSTI Identifier:
- 1885622
- Alternate Identifier(s):
- OSTI ID: 1885624; OSTI ID: 1888778
- Report Number(s):
- NREL/JA-2800-84058
Journal ID: ISSN 1742-464X
- Grant/Contract Number:
- DE‐AC36‐08GO28308; AC36-08GO28308; 2018-07152; 2018-04969; 2019-02496; 2015-009633; 1552355; PRG1540
- Resource Type:
- Published Article
- Journal Name:
- Federation of European Biochemical Societies (FEBS) Journal
- Additional Journal Information:
- Journal Name: Federation of European Biochemical Societies (FEBS) Journal Journal Volume: 290 Journal Issue: 2; Journal ID: ISSN 1742-464X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cel7; cellulase; fluorescence; ligand binding; Phanerochaete chrysosporium; Trichoderma reesei
Citation Formats
Haataja, Topi, Gado, Japheth E., Nutt, Anu, Anderson, Nolan T., Nilsson, Mikael, Momeni, Majid Haddad, Isaksson, Roland, Väljamäe, Priit, Johansson, Gunnar, Payne, Christina M., and Ståhlberg, Jerry. Enzyme kinetics by GH7 cellobiohydrolases on chromogenic substrates is dictated by non‐productive binding: insights from crystal structures and MD simulation. United Kingdom: N. p., 2022.
Web. doi:10.1111/febs.16602.
Haataja, Topi, Gado, Japheth E., Nutt, Anu, Anderson, Nolan T., Nilsson, Mikael, Momeni, Majid Haddad, Isaksson, Roland, Väljamäe, Priit, Johansson, Gunnar, Payne, Christina M., & Ståhlberg, Jerry. Enzyme kinetics by GH7 cellobiohydrolases on chromogenic substrates is dictated by non‐productive binding: insights from crystal structures and MD simulation. United Kingdom. https://doi.org/10.1111/febs.16602
Haataja, Topi, Gado, Japheth E., Nutt, Anu, Anderson, Nolan T., Nilsson, Mikael, Momeni, Majid Haddad, Isaksson, Roland, Väljamäe, Priit, Johansson, Gunnar, Payne, Christina M., and Ståhlberg, Jerry. Tue .
"Enzyme kinetics by GH7 cellobiohydrolases on chromogenic substrates is dictated by non‐productive binding: insights from crystal structures and MD simulation". United Kingdom. https://doi.org/10.1111/febs.16602.
@article{osti_1885622,
title = {Enzyme kinetics by GH7 cellobiohydrolases on chromogenic substrates is dictated by non‐productive binding: insights from crystal structures and MD simulation},
author = {Haataja, Topi and Gado, Japheth E. and Nutt, Anu and Anderson, Nolan T. and Nilsson, Mikael and Momeni, Majid Haddad and Isaksson, Roland and Väljamäe, Priit and Johansson, Gunnar and Payne, Christina M. and Ståhlberg, Jerry},
abstractNote = {Cellobiohydrolases (CBHs) in the glycoside hydrolase family 7 (GH7) ( EC3.2.1.176 ) are the major cellulose degrading enzymes both in industrial settings and in the context of carbon cycling in nature. Small carbohydrate conjugates such as p‐ nitrophenyl‐β‐ d ‐cellobioside (pNPC), p‐ nitrophenyl‐β‐ d ‐lactoside (pNPL) and methylumbelliferyl‐β‐ d ‐cellobioside have commonly been used in colorimetric and fluorometric assays for analysing activity of these enzymes. Despite the similar nature of these compounds the kinetics of their enzymatic hydrolysis vary greatly between the different compounds as well as among different enzymes within the GH7 family. Through enzyme kinetics, crystallographic structure determination, molecular dynamics simulations, and fluorometric binding studies using the closely related compound o‐nitrophenyl‐β‐ d ‐cellobioside (oNPC), in this work we examine the different hydrolysis characteristics of these compounds on two model enzymes of this class, TrCel7A from Trichoderma reesei and PcCel7D from Phanerochaete chrysosporium . Protein crystal structures of the E212Q mutant of TrCel7A with pNPC and pNPL, and the wildtype TrCel7A with oNPC, reveal that non‐productive binding at the product site is the dominating binding mode for these compounds. Enzyme kinetics results suggest the strength of non‐productive binding is a key determinant for the activity characteristics on these substrates, with PcCel7D consistently showing higher turnover rates ( k cat ) than TrCel7A, but higher Michaelis–Menten ( K M ) constants as well. Furthermore, oNPC turned out to be useful as an active‐site probe for fluorometric determination of the dissociation constant for cellobiose on TrCel7A but could not be utilized for the same purpose on PcCel7D, likely due to strong binding to an unknown site outside the active site.},
doi = {10.1111/febs.16602},
journal = {Federation of European Biochemical Societies (FEBS) Journal},
number = 2,
volume = 290,
place = {United Kingdom},
year = {Tue Sep 06 00:00:00 EDT 2022},
month = {Tue Sep 06 00:00:00 EDT 2022}
}
https://doi.org/10.1111/febs.16602
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