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Title: Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG

Abstract

Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by glutathione S-transferases (GSTs) has been reported in several sphingomonads. Here in this paper, we apply quantum mechanics/molecular mechanics simulations to study the mechanism of two glutathione-dependent enzymes in the β-aryl ether catabolic pathway of Sphingomonas sp. SYK-6, namely, LigF, a β-etherase, and LigG, a lyase. For LigF, the free-energy landscape supports a SN2 reaction mechanism, with the monoaromatic leaving group being promptly neutralized upon release. Specific interactions with conserved residues are responsible for stereoselectivity and for activation of the cofactor as a nucleophile. A glutathione conjugate is also released by LigF and serves the substrate of LigG, undergoing a SN2-like reaction, in which Cys15 acts as the nucleophile, to yield the second monoaromatic product. The simulations suggest that the electron-donating substituent at the para-position found in lignin-derived aromatics and the interaction with Tyr217 are essential for reactivity in LigG. Overall, this work deepens the understanding of the stereospecific enzymatic mechanisms in the β-aryl ether cleavage pathway and reveals key structural features underpinning the ligninolytic activity detected in several sphingomonadmore » GSTs.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States). National Bioenergy Center; Univ. of Campinas (UNICAMP), Sao Paulo (Brazil). Inst. of Chemistry and Center for Computing in Engineering and Sciences
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
  3. Univ. of Campinas (UNICAMP), Sao Paulo (Brazil). Inst. of Chemistry and Center for Computing in Engineering and Sciences
  4. National Renewable Energy Lab. (NREL), Golden, CO (United States). National Bioenergy Center
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office; USDOE Office of Science (SC), Biological and Environmental Research (BER); São Paulo Research Foundation (FAPESP)
OSTI Identifier:
1578254
Alternate Identifier(s):
OSTI ID: 1607161
Report Number(s):
NREL/JA-2700-75435
Journal ID: ISSN 1520-6106
Grant/Contract Number:  
AC36-08GO28308; 2016/04775-5; 2013/08293-7; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry
Additional Journal Information:
Journal Volume: 123; Journal Issue: 48; Journal ID: ISSN 1520-6106
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; lignin; enzyme; mechanism; qmmm; molecular modeling; BCPL

Citation Formats

Prates, Erica Teixeira, Crowley, Michael F., Skaf, Munir S., and Beckham, Gregg T. Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG. United States: N. p., 2019. Web. doi:10.1021/acs.jpcb.9b06243.
Prates, Erica Teixeira, Crowley, Michael F., Skaf, Munir S., & Beckham, Gregg T. Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG. United States. https://doi.org/10.1021/acs.jpcb.9b06243
Prates, Erica Teixeira, Crowley, Michael F., Skaf, Munir S., and Beckham, Gregg T. Tue . "Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG". United States. https://doi.org/10.1021/acs.jpcb.9b06243. https://www.osti.gov/servlets/purl/1578254.
@article{osti_1578254,
title = {Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG},
author = {Prates, Erica Teixeira and Crowley, Michael F. and Skaf, Munir S. and Beckham, Gregg T.},
abstractNote = {Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by glutathione S-transferases (GSTs) has been reported in several sphingomonads. Here in this paper, we apply quantum mechanics/molecular mechanics simulations to study the mechanism of two glutathione-dependent enzymes in the β-aryl ether catabolic pathway of Sphingomonas sp. SYK-6, namely, LigF, a β-etherase, and LigG, a lyase. For LigF, the free-energy landscape supports a SN2 reaction mechanism, with the monoaromatic leaving group being promptly neutralized upon release. Specific interactions with conserved residues are responsible for stereoselectivity and for activation of the cofactor as a nucleophile. A glutathione conjugate is also released by LigF and serves the substrate of LigG, undergoing a SN2-like reaction, in which Cys15 acts as the nucleophile, to yield the second monoaromatic product. The simulations suggest that the electron-donating substituent at the para-position found in lignin-derived aromatics and the interaction with Tyr217 are essential for reactivity in LigG. Overall, this work deepens the understanding of the stereospecific enzymatic mechanisms in the β-aryl ether cleavage pathway and reveals key structural features underpinning the ligninolytic activity detected in several sphingomonad GSTs.},
doi = {10.1021/acs.jpcb.9b06243},
journal = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},
number = 48,
volume = 123,
place = {United States},
year = {Tue Nov 05 00:00:00 EST 2019},
month = {Tue Nov 05 00:00:00 EST 2019}
}

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