Characterization of alkylguaiacol-degrading cytochromes P450 for the biocatalytic valorization of lignin
Abstract
Upgrading lignin, an underutilized component of biomass, is essential for the sustainability of biorefineries. Biocatalysis has considerable potential for upgrading lignin, but our lack of knowledge of relevant enzymes and pathways has limited its application. Herein, we describe a microbial pathway responsible for catabolizing alkylguaiacols, a major component of several industrial lignin streams. Catabolism is initiated by a cytochrome P450, with related P450s catalyzing the O-demethylation of different lignin-derived guaiacols and subsequent catabolism depending on the substitution pattern of the guaiacol. Importantly, the alkylguaiacol catabolic pathway enables bacterial growth on corn stover lignin produced by reductive catalytic fractionation. Overall, these insights greatly facilitate the engineering of P450s and bacteria to biocatalytically upgrade lignin.
- Authors:
-
- Univ. of British Columbia, Vancouver, BC (Canada)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO)
- OSTI Identifier:
- 1726039
- Report Number(s):
- NREL/JA-2800-77914
Journal ID: ISSN 0027-8424; MainId:31823;UUID:8ffde6ac-d3c6-4346-99c8-b37e82b09c30;MainAdminID:18846
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 117; Journal Issue: 41; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biocatalysis; cytochrome P450; guaiacol; lignin valorization; O-demethylase
Citation Formats
Fetherolf, Morgan M., Levy-Booth, David J., Navas, Laura E., Liu, Jie, Grigg, Jason C., Wilson, Andrew, Katahira, Rui, Beckham, Gregg T., Mohn, William W., and Eltis, Lindsay D. Characterization of alkylguaiacol-degrading cytochromes P450 for the biocatalytic valorization of lignin. United States: N. p., 2020.
Web. doi:10.1073/pnas.1916349117.
Fetherolf, Morgan M., Levy-Booth, David J., Navas, Laura E., Liu, Jie, Grigg, Jason C., Wilson, Andrew, Katahira, Rui, Beckham, Gregg T., Mohn, William W., & Eltis, Lindsay D. Characterization of alkylguaiacol-degrading cytochromes P450 for the biocatalytic valorization of lignin. United States. https://doi.org/10.1073/pnas.1916349117
Fetherolf, Morgan M., Levy-Booth, David J., Navas, Laura E., Liu, Jie, Grigg, Jason C., Wilson, Andrew, Katahira, Rui, Beckham, Gregg T., Mohn, William W., and Eltis, Lindsay D. Mon .
"Characterization of alkylguaiacol-degrading cytochromes P450 for the biocatalytic valorization of lignin". United States. https://doi.org/10.1073/pnas.1916349117. https://www.osti.gov/servlets/purl/1726039.
@article{osti_1726039,
title = {Characterization of alkylguaiacol-degrading cytochromes P450 for the biocatalytic valorization of lignin},
author = {Fetherolf, Morgan M. and Levy-Booth, David J. and Navas, Laura E. and Liu, Jie and Grigg, Jason C. and Wilson, Andrew and Katahira, Rui and Beckham, Gregg T. and Mohn, William W. and Eltis, Lindsay D.},
abstractNote = {Upgrading lignin, an underutilized component of biomass, is essential for the sustainability of biorefineries. Biocatalysis has considerable potential for upgrading lignin, but our lack of knowledge of relevant enzymes and pathways has limited its application. Herein, we describe a microbial pathway responsible for catabolizing alkylguaiacols, a major component of several industrial lignin streams. Catabolism is initiated by a cytochrome P450, with related P450s catalyzing the O-demethylation of different lignin-derived guaiacols and subsequent catabolism depending on the substitution pattern of the guaiacol. Importantly, the alkylguaiacol catabolic pathway enables bacterial growth on corn stover lignin produced by reductive catalytic fractionation. Overall, these insights greatly facilitate the engineering of P450s and bacteria to biocatalytically upgrade lignin.},
doi = {10.1073/pnas.1916349117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 117,
place = {United States},
year = {Mon Sep 28 00:00:00 EDT 2020},
month = {Mon Sep 28 00:00:00 EDT 2020}
}
Works referenced in this record:
Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014
- Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
- Science, Vol. 344, Issue 6185, p. 1246843-1246843
Purification and characterization of cytochrome P450RR1 from Rhodococcus rhodochrous
journal, April 1993
- Eltis, Lindsay D.; Karlson, Ulrich; Timmis, Kenneth N.
- European Journal of Biochemistry, Vol. 213, Issue 1
Identification of the two-component guaiacol demethylase system from Rhodococcus rhodochrous and expression in Pseudomonas putida EM42 for guaiacol assimilation
journal, March 2019
- García-Hidalgo, Javier; Ravi, Krithika; Kuré, Lise-Lotte
- AMB Express, Vol. 9, Issue 1
Reductive Catalytic Fractionation of Corn Stover Lignin
journal, October 2016
- Anderson, Eric M.; Katahira, Rui; Reed, Michelle
- ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 12
Spectroscopic features of cytochrome P450 reaction intermediates
journal, March 2011
- Luthra, Abhinav; Denisov, Ilia G.; Sligar, Stephen G.
- Archives of Biochemistry and Biophysics, Vol. 507, Issue 1
Bright Side of Lignin Depolymerization: Toward New Platform Chemicals
journal, January 2018
- Sun, Zhuohua; Fridrich, Bálint; de Santi, Alessandra
- Chemical Reviews, Vol. 118, Issue 2
Process Design and Economics for the Conversion of Lignocellulosic Biomass to Hydrocarbons: Dilute-Acid and Enzymatic Deconstruction of Biomass to Sugars and Biological Conversion of Sugars to Hydrocarbons
report, October 2013
- Davis, R.; Tao, L.; Tan, E. C. D.
- NREL/TP-5100-60223
Vanillate O-demethylase from Pseudomonas species
book, January 1988
- Buswell, John A.; Ribbons, Douglas W.
- Methods in Enzymology
Reductive lignocellulose fractionation into soluble lignin-derived phenolic monomers and dimers and processable carbohydrate pulps
journal, January 2015
- Van den Bosch, S.; Schutyser, W.; Vanholme, R.
- Energy & Environmental Science, Vol. 8, Issue 6
The Catalytic Valorization of Lignin for the Production of Renewable Chemicals
journal, June 2010
- Zakzeski, Joseph; Bruijnincx, Pieter C. A.; Jongerius, Anna L.
- Chemical Reviews, Vol. 110, Issue 6, p. 3552-3599
Opportunities and challenges in biological lignin valorization
journal, December 2016
- Beckham, Gregg T.; Johnson, Christopher W.; Karp, Eric M.
- Current Opinion in Biotechnology, Vol. 42
Adipic acid production from lignin
journal, January 2015
- Vardon, Derek R.; Franden, Mary Ann; Johnson, Christopher W.
- Energy & Environmental Science, Vol. 8, Issue 2
Catabolism of Alkylphenols in Rhodococcus via a Meta-Cleavage Pathway Associated With Genomic Islands
journal, August 2019
- Levy-Booth, David J.; Fetherolf, Morgan M.; Stewart, Gordon R.
- Frontiers in Microbiology, Vol. 10
Structure of aryl O -demethylase offers molecular insight into a catalytic tyrosine-dependent mechanism
journal, April 2017
- Kohler, Amanda C.; Mills, Matthew J. L.; Adams, Paul D.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 16
The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse
journal, October 2006
- McLeod, M. P.; Warren, R. L.; Hsiao, W. W. L.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 42, p. 15582-15587
Catabolism of Benzoate and Phthalate in Rhodococcus sp. Strain RHA1: Redundancies and Convergence
journal, June 2005
- Patrauchan, M. A.; Florizone, C.; Dosanjh, M.
- Journal of Bacteriology, Vol. 187, Issue 12, p. 4050-4063
Cloning and sequencing of Pseudomonas genes encoding vanillate demethylase.
journal, October 1988
- Brunel, F.; Davison, J.
- Journal of Bacteriology, Vol. 170, Issue 10
Characterization of p-Hydroxycinnamate Catabolism in a Soil Actinobacterium
journal, September 2014
- Otani, H.; Lee, Y. -E.; Casabon, I.
- Journal of Bacteriology, Vol. 196, Issue 24
Enabling microbial syringol conversion through structure-guided protein engineering
journal, June 2019
- Machovina, Melodie M.; Mallinson, Sam J. B.; Knott, Brandon C.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 28
Characterization and Evolution of Anthranilate 1,2-Dioxygenase from Acinetobacter sp. Strain ADP1
journal, January 2001
- Eby, D. M.; Beharry, Z. M.; Coulter, E. D.
- Journal of Bacteriology, Vol. 183, Issue 1
A promiscuous cytochrome P450 aromatic O-demethylase for lignin bioconversion
journal, June 2018
- Mallinson, Sam J. B.; Machovina, Melodie M.; Silveira, Rodrigo L.
- Nature Communications, Vol. 9, Issue 1
Oxidative demethylation of algal carbohydrates by cytochrome P450 monooxygenases
journal, February 2018
- Reisky, Lukas; Büchsenschütz, Hanna C.; Engel, Jennifer
- Nature Chemical Biology, Vol. 14, Issue 4
Cytochrome P450 of wood-rotting basidiomycetes and biotechnological applications: Cytochrome P450s of Basidiomycetes
journal, January 2013
- Ichinose, Hirofumi
- Biotechnology and Applied Biochemistry, Vol. 60, Issue 1
Enhancing muconic acid production from glucose and lignin-derived aromatic compounds via increased protocatechuate decarboxylase activity
journal, December 2016
- Johnson, Christopher W.; Salvachúa, Davinia; Khanna, Payal
- Metabolic Engineering Communications, Vol. 3
Three-dimensional structure of NADPH-cytochrome P450 reductase: Prototype for FMN- and FAD-containing enzymes
journal, August 1997
- Wang, M.; Roberts, D. L.; Paschke, R.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 16
Paving the Way for Lignin Valorisation: Recent Advances in Bioengineering, Biorefining and Catalysis
journal, June 2016
- Rinaldi, Roberto; Jastrzebski, Robin; Clough, Matthew T.
- Angewandte Chemie International Edition, Vol. 55, Issue 29
Life cycle assessment of adipic acid production from lignin
journal, January 2018
- Corona, Andrea; Biddy, Mary J.; Vardon, Derek R.
- Green Chemistry, Vol. 20, Issue 16
Lignin valorization through integrated biological funneling and chemical catalysis
journal, August 2014
- Linger, J. G.; Vardon, D. R.; Guarnieri, M. T.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018
A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products
journal, November 2019
- Becker, Judith; Wittmann, Christoph
- Biotechnology Advances, Vol. 37, Issue 6
Chemicals from lignin: an interplay of lignocellulose fractionation, depolymerisation, and upgrading
journal, January 2018
- Schutyser, W.; Renders, T.; Van den Bosch, S.
- Chemical Society Reviews, Vol. 47, Issue 3
Phenol and cresol metabolism inBacillus pumilus isolated from contaminated groundwater
journal, January 1995
- Günther, K.; Schlosser, D.; Fritsche, W.
- Journal of Basic Microbiology, Vol. 35, Issue 2
Two independently regulated cytochromes P-450 in a Rhodococcus rhodochrous strain that degrades 2-ethoxyphenol and 4-methoxybenzoate.
journal, March 1993
- Karlson, U.; Dwyer, D. F.; Hooper, S. W.
- Journal of Bacteriology, Vol. 175, Issue 5
The crystal structure of a new O ‐demethylase from Sphingobium sp. strain SYK ‐6
journal, May 2017
- Harada, Ayaka; Kamimura, Naofumi; Takeuchi, Koh
- The FEBS Journal, Vol. 284, Issue 12
Development of an Improved System for the Generation of Knockout Mutants of Amycolatopsis sp. Strain ATCC 39116
journal, December 2016
- Meyer, Florian; Pupkes, Hilke; Steinbüchel, Alexander
- Applied and Environmental Microbiology, Vol. 83, Issue 3
Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds
journal, January 2007
- Masai, Eiji; Katayama, Yoshihiro; Fukuda, Masao
- Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 1
A sustainable wood biorefinery for low–carbon footprint chemicals production
journal, February 2020
- Liao, Yuhe; Koelewijn, Steven-Friso; Van den Bossche, Gil
- Science, Vol. 367, Issue 6484
Intradiol pathway ofpara-cresol conversion byRhodococcus opacus 1CP
journal, July 2007
- Kolomytseva, Marina P.; Baskunov, Boris P.; Golovleva, Ludmila Alexeevna
- Biotechnology Journal, Vol. 2, Issue 7
Vanillin Catabolism in Rhodococcus jostii RHA1
journal, November 2011
- Chen, Hao-Ping; Chow, Mindy; Liu, Chi-Chun
- Applied and Environmental Microbiology, Vol. 78, Issue 2
The Ins and Outs of Ring-Cleaving Dioxygenases
journal, January 2006
- Vaillancourt, Frédéric H.; Bolin, Jeffrey T.; Eltis, Lindsay D.
- Critical Reviews in Biochemistry and Molecular Biology, Vol. 41, Issue 4
Bioprocess development for muconic acid production from aromatic compounds and lignin
journal, January 2018
- Salvachúa, Davinia; Johnson, Christopher W.; Singer, Christine A.
- Green Chemistry, Vol. 20, Issue 21
(+)-γ-Carboxymethyl-γ-methyl-Δα-butenolide. A 1,2 ring-fission product of 4-methylcatechol by Pseudomonas desmolyticum
journal, January 1971
- Catelani, D.; Fiecchi, A.; Galli, E.
- Biochemical Journal, Vol. 121, Issue 1