Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics

Sulfolane is an industrial solvent and emerging organic contaminant affecting groundwater around the world, but little is known about microbes capable of biodegrading sulfolane or the pathways involved. We combined DNA-based stable isotope probing (SIP) with genome-resolved metagenomics to identify...

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Published in:Scientific Reports
Main Authors: Kasanke, Christopher Paul, Collins, R. Eric, Leigh, Mary Beth
Format: Text
Language:English
Published: Nature Publishing Group UK 2019
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395730/
http://www.ncbi.nlm.nih.gov/pubmed/30816276
https://doi.org/10.1038/s41598-019-40000-2
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spelling ftpubmed:oai:pubmedcentral.nih.gov:6395730 2023-05-15T18:28:27+02:00 Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics Kasanke, Christopher Paul Collins, R. Eric Leigh, Mary Beth 2019-02-28 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395730/ http://www.ncbi.nlm.nih.gov/pubmed/30816276 https://doi.org/10.1038/s41598-019-40000-2 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395730/ http://www.ncbi.nlm.nih.gov/pubmed/30816276 http://dx.doi.org/10.1038/s41598-019-40000-2 © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. CC-BY Article Text 2019 ftpubmed https://doi.org/10.1038/s41598-019-40000-2 2019-03-10T01:17:22Z Sulfolane is an industrial solvent and emerging organic contaminant affecting groundwater around the world, but little is known about microbes capable of biodegrading sulfolane or the pathways involved. We combined DNA-based stable isotope probing (SIP) with genome-resolved metagenomics to identify microorganisms associated with sulfolane biodegradation in a contaminated subarctic aquifer. In addition to 16S rRNA gene amplicon sequencing, we performed shotgun metagenomics on the (13)C-labeled DNA to obtain functional and taxonomic information about the active sulfolane-degrading community. We identified the primary sulfolane degrader, comprising ~85% of the labeled community in the amplicon sequencing dataset, as closely related to Rhodoferax ferrireducens strain T118. We obtained a 99.8%-complete metagenome-assembled genome for this strain, allowing us to identify putative pathways of sulfolane biodegradation. Although the 4S dibenzothiophene desulfurization pathway has been proposed as an analog for sulfolane biodegradation, we found only a subset of the required genes, suggesting a novel pathway specific to sulfolane. DszA, the enzyme likely responsible for opening the sulfolane ring structure, was encoded on both the chromosome and a plasmid. This study demonstrates the power of integrating DNA-SIP with metagenomics to characterize emerging organic contaminant degraders without culture bias and expands the known taxonomic distribution of sulfolane biodegradation. Text Subarctic PubMed Central (PMC) Scientific Reports 9 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Article
spellingShingle Article
Kasanke, Christopher Paul
Collins, R. Eric
Leigh, Mary Beth
Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
topic_facet Article
description Sulfolane is an industrial solvent and emerging organic contaminant affecting groundwater around the world, but little is known about microbes capable of biodegrading sulfolane or the pathways involved. We combined DNA-based stable isotope probing (SIP) with genome-resolved metagenomics to identify microorganisms associated with sulfolane biodegradation in a contaminated subarctic aquifer. In addition to 16S rRNA gene amplicon sequencing, we performed shotgun metagenomics on the (13)C-labeled DNA to obtain functional and taxonomic information about the active sulfolane-degrading community. We identified the primary sulfolane degrader, comprising ~85% of the labeled community in the amplicon sequencing dataset, as closely related to Rhodoferax ferrireducens strain T118. We obtained a 99.8%-complete metagenome-assembled genome for this strain, allowing us to identify putative pathways of sulfolane biodegradation. Although the 4S dibenzothiophene desulfurization pathway has been proposed as an analog for sulfolane biodegradation, we found only a subset of the required genes, suggesting a novel pathway specific to sulfolane. DszA, the enzyme likely responsible for opening the sulfolane ring structure, was encoded on both the chromosome and a plasmid. This study demonstrates the power of integrating DNA-SIP with metagenomics to characterize emerging organic contaminant degraders without culture bias and expands the known taxonomic distribution of sulfolane biodegradation.
format Text
author Kasanke, Christopher Paul
Collins, R. Eric
Leigh, Mary Beth
author_facet Kasanke, Christopher Paul
Collins, R. Eric
Leigh, Mary Beth
author_sort Kasanke, Christopher Paul
title Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
title_short Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
title_full Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
title_fullStr Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
title_full_unstemmed Identification and Characterization of a Dominant Sulfolane-Degrading Rhodoferax sp. via Stable Isotope Probing Combined with Metagenomics
title_sort identification and characterization of a dominant sulfolane-degrading rhodoferax sp. via stable isotope probing combined with metagenomics
publisher Nature Publishing Group UK
publishDate 2019
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395730/
http://www.ncbi.nlm.nih.gov/pubmed/30816276
https://doi.org/10.1038/s41598-019-40000-2
genre Subarctic
genre_facet Subarctic
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395730/
http://www.ncbi.nlm.nih.gov/pubmed/30816276
http://dx.doi.org/10.1038/s41598-019-40000-2
op_rights © The Author(s) 2019
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1038/s41598-019-40000-2
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