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

Abstract

ABSTRACT 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 palustrisCGA009 is a known degrader of phenolic compounds under photoheterotrophic conditions via the benzoyl coenzyme A (CoA) degradation (BAD) pathway. However,R. palustrisCGA009 is reported to be unable to metabolizemeta-methoxylated phenolics, such as syringic acid. We isolated a strain ofR. 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 thevanARBoperon (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 avanARBdeletion mutant demonstrated the involvement of thevanARBoperon in anaerobic syringic acid degradation. These observations providemore » new insights into the anaerobic degradation ofmeta-methoxylated and other aromatics byR. palustris. IMPORTANCELignin 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 aRhodopseudomonas palustrisstrain capable of syringic acid degradation reveal a previously unknown metabolic route for aromatic degradation inR. 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.« less

Authors:
; ; ; ; ; ; ; ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1592503
Alternate Identifier(s):
OSTI ID: 1579365
Grant/Contract Number:  
SC0018409; FC02-07ER64494; AC02-05CH11231; CBET-1506820; T32GM008349
Resource Type:
Published Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Name: Applied and Environmental Microbiology Journal Volume: 86 Journal Issue: 3; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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., and Nojiri, Hideaki. Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris. United States: N. p., 2019. Web. doi:10.1128/AEM.01888-19.
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., & Nojiri, Hideaki. Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris. United States. doi:10.1128/AEM.01888-19.
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., and Nojiri, Hideaki. Fri . "Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris". United States. doi:10.1128/AEM.01888-19.
@article{osti_1592503,
title = {Anaerobic Degradation of Syringic Acid by an Adapted Strain of Rhodopseudomonas palustris},
author = {Oshlag, J. Zachary and Ma, Yanjun and Morse, Kaitlin and Burger, Brian T. and Lemke, Rachelle A. and Karlen, Steven D. and Myers, Kevin S. and Donohue, Timothy J. and Noguera, Daniel R. and Nojiri, Hideaki},
abstractNote = {ABSTRACT 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 palustrisCGA009 is a known degrader of phenolic compounds under photoheterotrophic conditions via the benzoyl coenzyme A (CoA) degradation (BAD) pathway. However,R. palustrisCGA009 is reported to be unable to metabolizemeta-methoxylated phenolics, such as syringic acid. We isolated a strain ofR. 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 thevanARBoperon (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 avanARBdeletion mutant demonstrated the involvement of thevanARBoperon in anaerobic syringic acid degradation. These observations provide new insights into the anaerobic degradation ofmeta-methoxylated and other aromatics byR. palustris. IMPORTANCELignin 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 aRhodopseudomonas palustrisstrain capable of syringic acid degradation reveal a previously unknown metabolic route for aromatic degradation inR. 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.},
doi = {10.1128/AEM.01888-19},
journal = {Applied and Environmental Microbiology},
number = 3,
volume = 86,
place = {United States},
year = {2019},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1128/AEM.01888-19

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