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Title: Characterization and engineering of a two-enzyme system for plastics depolymerization

Abstract

Plastics pollution represents a global environmental crisis. In response, microbes are evolving the capacity to utilize synthetic polymers as carbon and energy sources. Recently,Ideonella sakaiensiswas reported to secrete a two-enzyme system to deconstruct polyethylene terephthalate (PET) to its constituent monomers. Specifically, theI. sakaiensisPETase depolymerizes PET, liberating soluble products, including mono(2-hydroxyethyl) terephthalate (MHET), which is cleaved to terephthalic acid and ethylene glycol by MHETase. Here, we report a 1.6 Å resolution MHETase structure, illustrating that the MHETase core domain is similar to PETase, capped by a lid domain. Simulations of the catalytic itinerary predict that MHETase follows the canonical two-step serine hydrolase mechanism. Bioinformatics analysis suggests that MHETase evolved from ferulic acid esterases, and two homologous enzymes are shown to exhibit MHET turnover. Analysis of the two homologous enzymes and the MHETase S131G mutant demonstrates the importance of this residue for accommodation of MHET in the active site. We also demonstrate that the MHETase lid is crucial for hydrolysis of MHET and, furthermore, that MHETase does not turnover mono(2-hydroxyethyl)-furanoate or mono(2-hydroxyethyl)-isophthalate. A highly synergistic relationship between PETase and MHETase was observed for the conversion of amorphous PET film to monomers across all nonzero MHETase concentrations tested. Finally, we compare the performancemore » of MHETase:PETase chimeric proteins of varying linker lengths, which all exhibit improved PET and MHET turnover relative to the free enzymes. Together, these results offer insights into the two-enzyme PET depolymerization system and will inform future efforts in the biological deconstruction and upcycling of mixed plastics.« less

Authors:
; ORCiD logo; ; ; ORCiD logo; ; ; ; ; ; ; ORCiD logo; ORCiD logo; ; ; ; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Energy Efficiency Office. Advanced Manufacturing Office; USDOE Office of Energy Efficiency and Renewable Energy (EERE), Energy Efficiency Office. Building Technologies Office; USDOE Laboratory Directed Research and Development (LDRD) Program; Research England; Biotechnology and Biological Sciences Research Council (BBSRC); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1668418
Alternate Identifier(s):
OSTI ID: 1772992
Report Number(s):
NREL/JA-2A00-76584
Journal ID: ISSN 0027-8424; /pnas/117/41/25476.atom
Grant/Contract Number:  
AC36-08GO28308; SC0011297TDD; BB/P011918/1; 3900101301; SC0011297; 1R01GM129519-01; CHE-1464946; CBET-1552355; MCB-1714556
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 117 Journal Issue: 41; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; polyethylene terephthalate; recycling; upcycling; biodegradation; serine hydrolase; polyester

Citation Formats

Knott, Brandon C., Erickson, Erika, Allen, Mark D., Gado, Japheth E., Graham, Rosie, Kearns, Fiona L., Pardo, Isabel, Topuzlu, Ece, Anderson, Jared J., Austin, Harry P., Dominick, Graham, Johnson, Christopher W., Rorrer, Nicholas A., Szostkiewicz, Caralyn J., Copié, Valérie, Payne, Christina M., Woodcock, H. Lee, Donohoe, Bryon S., Beckham, Gregg T., and McGeehan, John E. Characterization and engineering of a two-enzyme system for plastics depolymerization. United States: N. p., 2020. Web. https://doi.org/10.1073/pnas.2006753117.
Knott, Brandon C., Erickson, Erika, Allen, Mark D., Gado, Japheth E., Graham, Rosie, Kearns, Fiona L., Pardo, Isabel, Topuzlu, Ece, Anderson, Jared J., Austin, Harry P., Dominick, Graham, Johnson, Christopher W., Rorrer, Nicholas A., Szostkiewicz, Caralyn J., Copié, Valérie, Payne, Christina M., Woodcock, H. Lee, Donohoe, Bryon S., Beckham, Gregg T., & McGeehan, John E. Characterization and engineering of a two-enzyme system for plastics depolymerization. United States. https://doi.org/10.1073/pnas.2006753117
Knott, Brandon C., Erickson, Erika, Allen, Mark D., Gado, Japheth E., Graham, Rosie, Kearns, Fiona L., Pardo, Isabel, Topuzlu, Ece, Anderson, Jared J., Austin, Harry P., Dominick, Graham, Johnson, Christopher W., Rorrer, Nicholas A., Szostkiewicz, Caralyn J., Copié, Valérie, Payne, Christina M., Woodcock, H. Lee, Donohoe, Bryon S., Beckham, Gregg T., and McGeehan, John E. Mon . "Characterization and engineering of a two-enzyme system for plastics depolymerization". United States. https://doi.org/10.1073/pnas.2006753117.
@article{osti_1668418,
title = {Characterization and engineering of a two-enzyme system for plastics depolymerization},
author = {Knott, Brandon C. and Erickson, Erika and Allen, Mark D. and Gado, Japheth E. and Graham, Rosie and Kearns, Fiona L. and Pardo, Isabel and Topuzlu, Ece and Anderson, Jared J. and Austin, Harry P. and Dominick, Graham and Johnson, Christopher W. and Rorrer, Nicholas A. and Szostkiewicz, Caralyn J. and Copié, Valérie and Payne, Christina M. and Woodcock, H. Lee and Donohoe, Bryon S. and Beckham, Gregg T. and McGeehan, John E.},
abstractNote = {Plastics pollution represents a global environmental crisis. In response, microbes are evolving the capacity to utilize synthetic polymers as carbon and energy sources. Recently,Ideonella sakaiensiswas reported to secrete a two-enzyme system to deconstruct polyethylene terephthalate (PET) to its constituent monomers. Specifically, theI. sakaiensisPETase depolymerizes PET, liberating soluble products, including mono(2-hydroxyethyl) terephthalate (MHET), which is cleaved to terephthalic acid and ethylene glycol by MHETase. Here, we report a 1.6 Å resolution MHETase structure, illustrating that the MHETase core domain is similar to PETase, capped by a lid domain. Simulations of the catalytic itinerary predict that MHETase follows the canonical two-step serine hydrolase mechanism. Bioinformatics analysis suggests that MHETase evolved from ferulic acid esterases, and two homologous enzymes are shown to exhibit MHET turnover. Analysis of the two homologous enzymes and the MHETase S131G mutant demonstrates the importance of this residue for accommodation of MHET in the active site. We also demonstrate that the MHETase lid is crucial for hydrolysis of MHET and, furthermore, that MHETase does not turnover mono(2-hydroxyethyl)-furanoate or mono(2-hydroxyethyl)-isophthalate. A highly synergistic relationship between PETase and MHETase was observed for the conversion of amorphous PET film to monomers across all nonzero MHETase concentrations tested. Finally, we compare the performance of MHETase:PETase chimeric proteins of varying linker lengths, which all exhibit improved PET and MHET turnover relative to the free enzymes. Together, these results offer insights into the two-enzyme PET depolymerization system and will inform future efforts in the biological deconstruction and upcycling of mixed plastics.},
doi = {10.1073/pnas.2006753117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 117,
place = {United States},
year = {2020},
month = {9}
}

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https://doi.org/10.1073/pnas.2006753117

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