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Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris

While lignin represents a major fraction of the carbon in plant biomass, biological strategies to convert the components of this heterogeneous polymer into products of industrial and biotechnological value are lacking. Syringic acid (3,5-dimethoxy-4-hydroxybenzoic acid) is a by-product of lignin deg...

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Autores principales: Oshlag, J. Zachary, Ma, Yanjun, Morse, Kaitlin, Burger, Brian T., Lemke, Rachelle A., Karlen, Steven D., Myers, Kevin S., Donohue, Timothy J., Noguera, Daniel R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974649/
https://www.ncbi.nlm.nih.gov/pubmed/31732577
http://dx.doi.org/10.1128/AEM.01888-19
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author Oshlag, J. Zachary
Ma, Yanjun
Morse, Kaitlin
Burger, Brian T.
Lemke, Rachelle A.
Karlen, Steven D.
Myers, Kevin S.
Donohue, Timothy J.
Noguera, Daniel R.
author_facet Oshlag, J. Zachary
Ma, Yanjun
Morse, Kaitlin
Burger, Brian T.
Lemke, Rachelle A.
Karlen, Steven D.
Myers, Kevin S.
Donohue, Timothy J.
Noguera, Daniel R.
author_sort Oshlag, J. Zachary
collection PubMed
description While lignin represents a major fraction of the carbon in plant biomass, biological strategies to convert the components of this heterogeneous polymer into products of industrial and biotechnological value are lacking. Syringic acid (3,5-dimethoxy-4-hydroxybenzoic acid) is a by-product of lignin degradation, appearing in lignocellulosic hydrolysates, deconstructed lignin streams, and other agricultural products. Rhodopseudomonas palustris CGA009 is a known degrader of phenolic compounds under photoheterotrophic conditions via the benzoyl coenzyme A (CoA) degradation (BAD) pathway. However, R. palustris CGA009 is reported to be unable to metabolize meta-methoxylated phenolics, such as syringic acid. We isolated a strain of R. palustris (strain SA008.1.07), adapted from CGA009, which can grow on syringic acid under photoheterotrophic conditions, utilizing it as a sole source of organic carbon and reducing power. An SA008.1.07 mutant with an inactive benzoyl-CoA reductase structural gene was able to grow on syringic acid, demonstrating that the metabolism of this aromatic compound is not through the BAD pathway. Comparative gene expression analyses of SA008.1.07 implicated the involvement of products of the vanARB operon (rpa3619, rpa3620, rpa3621), which has been described as catalyzing aerobic aromatic ring demethylation in other bacteria, in anaerobic syringic acid degradation. In addition, experiments with a vanARB deletion mutant demonstrated the involvement of the vanARB operon in anaerobic syringic acid degradation. These observations provide new insights into the anaerobic degradation of meta-methoxylated and other aromatics by R. palustris. IMPORTANCE Lignin is the most abundant aromatic polymer on Earth and a resource that could eventually substitute for fossil fuels as a source of aromatic compounds for industrial and biotechnological applications. Engineering microorganisms for the production of aromatic-based biochemicals requires detailed knowledge of the metabolic pathways for the degradation of aromatics that are present in lignin. Our isolation and analysis of a Rhodopseudomonas palustris strain capable of syringic acid degradation reveal a previously unknown metabolic route for aromatic degradation in R. palustris. This study highlights several key features of this pathway and sets the stage for a more complete understanding of the microbial metabolic repertoire required to metabolize aromatic compounds from lignin and other renewable sources.
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spelling pubmed-69746492020-02-04 Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris Oshlag, J. Zachary Ma, Yanjun Morse, Kaitlin Burger, Brian T. Lemke, Rachelle A. Karlen, Steven D. Myers, Kevin S. Donohue, Timothy J. Noguera, Daniel R. Appl Environ Microbiol Biodegradation While lignin represents a major fraction of the carbon in plant biomass, biological strategies to convert the components of this heterogeneous polymer into products of industrial and biotechnological value are lacking. Syringic acid (3,5-dimethoxy-4-hydroxybenzoic acid) is a by-product of lignin degradation, appearing in lignocellulosic hydrolysates, deconstructed lignin streams, and other agricultural products. Rhodopseudomonas palustris CGA009 is a known degrader of phenolic compounds under photoheterotrophic conditions via the benzoyl coenzyme A (CoA) degradation (BAD) pathway. However, R. palustris CGA009 is reported to be unable to metabolize meta-methoxylated phenolics, such as syringic acid. We isolated a strain of R. palustris (strain SA008.1.07), adapted from CGA009, which can grow on syringic acid under photoheterotrophic conditions, utilizing it as a sole source of organic carbon and reducing power. An SA008.1.07 mutant with an inactive benzoyl-CoA reductase structural gene was able to grow on syringic acid, demonstrating that the metabolism of this aromatic compound is not through the BAD pathway. Comparative gene expression analyses of SA008.1.07 implicated the involvement of products of the vanARB operon (rpa3619, rpa3620, rpa3621), which has been described as catalyzing aerobic aromatic ring demethylation in other bacteria, in anaerobic syringic acid degradation. In addition, experiments with a vanARB deletion mutant demonstrated the involvement of the vanARB operon in anaerobic syringic acid degradation. These observations provide new insights into the anaerobic degradation of meta-methoxylated and other aromatics by R. palustris. IMPORTANCE Lignin is the most abundant aromatic polymer on Earth and a resource that could eventually substitute for fossil fuels as a source of aromatic compounds for industrial and biotechnological applications. Engineering microorganisms for the production of aromatic-based biochemicals requires detailed knowledge of the metabolic pathways for the degradation of aromatics that are present in lignin. Our isolation and analysis of a Rhodopseudomonas palustris strain capable of syringic acid degradation reveal a previously unknown metabolic route for aromatic degradation in R. palustris. This study highlights several key features of this pathway and sets the stage for a more complete understanding of the microbial metabolic repertoire required to metabolize aromatic compounds from lignin and other renewable sources. American Society for Microbiology 2020-01-21 /pmc/articles/PMC6974649/ /pubmed/31732577 http://dx.doi.org/10.1128/AEM.01888-19 Text en Copyright © 2020 Oshlag et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biodegradation
Oshlag, J. Zachary
Ma, Yanjun
Morse, Kaitlin
Burger, Brian T.
Lemke, Rachelle A.
Karlen, Steven D.
Myers, Kevin S.
Donohue, Timothy J.
Noguera, Daniel R.
Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title_full Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title_fullStr Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title_full_unstemmed Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title_short Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris
title_sort anaerobic degradation of syringic acid by an adapted strain of rhodopseudomonas palustris
topic Biodegradation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974649/
https://www.ncbi.nlm.nih.gov/pubmed/31732577
http://dx.doi.org/10.1128/AEM.01888-19
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