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Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture

Polycyclic aromatic hydrocarbons (PAH) such as naphthalene are widespread, recalcitrant pollutants in anoxic and methanogenic environments. A mechanism catalyzing PAH activation under methanogenic conditions has yet to be discovered, and the microbial communities coordinating their metabolism are la...

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Autores principales: Toth, Courtney R. A., Berdugo-Clavijo, Carolina, O’Farrell, Corynne M., Jones, Gareth M., Sheremet, Andriy, Dunfield, Peter F., Gieg, Lisa M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6164631/
https://www.ncbi.nlm.nih.gov/pubmed/29996505
http://dx.doi.org/10.3390/microorganisms6030065
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author Toth, Courtney R. A.
Berdugo-Clavijo, Carolina
O’Farrell, Corynne M.
Jones, Gareth M.
Sheremet, Andriy
Dunfield, Peter F.
Gieg, Lisa M.
author_facet Toth, Courtney R. A.
Berdugo-Clavijo, Carolina
O’Farrell, Corynne M.
Jones, Gareth M.
Sheremet, Andriy
Dunfield, Peter F.
Gieg, Lisa M.
author_sort Toth, Courtney R. A.
collection PubMed
description Polycyclic aromatic hydrocarbons (PAH) such as naphthalene are widespread, recalcitrant pollutants in anoxic and methanogenic environments. A mechanism catalyzing PAH activation under methanogenic conditions has yet to be discovered, and the microbial communities coordinating their metabolism are largely unknown. This is primarily due to the difficulty of cultivating PAH degraders, requiring lengthy incubations to yield sufficient biomass for biochemical analysis. Here, we sought to characterize a new methanogenic naphthalene-degrading enrichment culture using DNA-based stable isotope probing (SIP) and metagenomic analyses. 16S rRNA gene sequencing of fractionated DNA pinpointed an unclassified Clostridiaceae species as a putative naphthalene degrader after two months of SIP incubation. This finding was supported by metabolite and metagenomic evidence of genes predicted to encode for enzymes facilitating naphthalene carboxylic acid CoA-thioesterification and degradation of an unknown arylcarboxyl-CoA structure. Our findings also suggest a possible but unknown role for Desulfuromonadales in naphthalene degradation. This is the first reported functional evidence of PAH biodegradation by a methanogenic consortium, and we envision that this approach could be used to assess carbon flow through other slow growing enrichment cultures and environmental samples.
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spelling pubmed-61646312018-10-10 Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture Toth, Courtney R. A. Berdugo-Clavijo, Carolina O’Farrell, Corynne M. Jones, Gareth M. Sheremet, Andriy Dunfield, Peter F. Gieg, Lisa M. Microorganisms Article Polycyclic aromatic hydrocarbons (PAH) such as naphthalene are widespread, recalcitrant pollutants in anoxic and methanogenic environments. A mechanism catalyzing PAH activation under methanogenic conditions has yet to be discovered, and the microbial communities coordinating their metabolism are largely unknown. This is primarily due to the difficulty of cultivating PAH degraders, requiring lengthy incubations to yield sufficient biomass for biochemical analysis. Here, we sought to characterize a new methanogenic naphthalene-degrading enrichment culture using DNA-based stable isotope probing (SIP) and metagenomic analyses. 16S rRNA gene sequencing of fractionated DNA pinpointed an unclassified Clostridiaceae species as a putative naphthalene degrader after two months of SIP incubation. This finding was supported by metabolite and metagenomic evidence of genes predicted to encode for enzymes facilitating naphthalene carboxylic acid CoA-thioesterification and degradation of an unknown arylcarboxyl-CoA structure. Our findings also suggest a possible but unknown role for Desulfuromonadales in naphthalene degradation. This is the first reported functional evidence of PAH biodegradation by a methanogenic consortium, and we envision that this approach could be used to assess carbon flow through other slow growing enrichment cultures and environmental samples. MDPI 2018-07-10 /pmc/articles/PMC6164631/ /pubmed/29996505 http://dx.doi.org/10.3390/microorganisms6030065 Text en © 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Toth, Courtney R. A.
Berdugo-Clavijo, Carolina
O’Farrell, Corynne M.
Jones, Gareth M.
Sheremet, Andriy
Dunfield, Peter F.
Gieg, Lisa M.
Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title_full Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title_fullStr Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title_full_unstemmed Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title_short Stable Isotope and Metagenomic Profiling of a Methanogenic Naphthalene-Degrading Enrichment Culture
title_sort stable isotope and metagenomic profiling of a methanogenic naphthalene-degrading enrichment culture
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6164631/
https://www.ncbi.nlm.nih.gov/pubmed/29996505
http://dx.doi.org/10.3390/microorganisms6030065
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