Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond

Oil sands process-affected water (OSPW), produced by surface-mining of oil sands in Canada, is alkaline and contains high concentrations of salts, metals, naphthenic acids, and polycyclic aromatic compounds (PAHs). Residual hydrocarbon biodegradation occurs naturally, but little is known about the h...

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Main Authors: Fauziah F. Rochman, Andriy Sheremet, Ivica Tamas, Alireza Saidi-Mehrabad, Joong-Jae Kim, Xiaoli Dong, Christoph W. Sensen, Lisa M. Gieg, Peter F. Dunfield
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01845/full
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spelling doaj-c5e4b2aa05e642cb8067e5b0d42c0a482020-11-24T23:21:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-09-01810.3389/fmicb.2017.01845272817Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings PondFauziah F. Rochman0Andriy Sheremet1Ivica Tamas2Ivica Tamas3Alireza Saidi-Mehrabad4Alireza Saidi-Mehrabad5Joong-Jae Kim6Xiaoli Dong7Xiaoli Dong8Christoph W. Sensen9Christoph W. Sensen10Lisa M. Gieg11Peter F. Dunfield12Department of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Novi Sad, SerbiaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biological Sciences, University of Alberta, Edmonton, AB, CanadaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biochemistry and Molecular Biology in the Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaDepartment of Geoscience, University of Calgary, Calgary, AB, CanadaDepartment of Biochemistry and Molecular Biology in the Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaInstitute of Computational Biotechnology, Graz University of Technology, Graz, AustriaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaOil sands process-affected water (OSPW), produced by surface-mining of oil sands in Canada, is alkaline and contains high concentrations of salts, metals, naphthenic acids, and polycyclic aromatic compounds (PAHs). Residual hydrocarbon biodegradation occurs naturally, but little is known about the hydrocarbon-degrading microbial communities present in OSPW. In this study, aerobic oxidation of benzene and naphthalene in the surface layer of an oil sands tailings pond were measured. The potential oxidation rates were 4.3 μmol L−1 OSPW d−1 for benzene and 21.4 μmol L−1 OSPW d−1 for naphthalene. To identify benzene and naphthalene-degrading microbial communities, metagenomics was combined with stable isotope probing (SIP), high-throughput sequencing of 16S rRNA gene amplicons, and isolation of microbial strains. SIP using 13C-benzene and 13C-naphthalene detected strains of the genera Methyloversatilis and Zavarzinia as the main benzene degraders, while strains belonging to the family Chromatiaceae and the genus Thauera were the main naphthalene degraders. Metagenomic analysis revealed a diversity of genes encoding oxygenases active against aromatic compounds. Although these genes apparently belonged to many phylogenetically diverse taxa, only a few of these taxa were predominant in the SIP experiments. This suggested that many members of the community are adapted to consuming other aromatic compounds, or are active only under specific conditions. 16S rRNA gene sequence datasets have been submitted to the Sequence Read Archive (SRA) under accession number SRP109130. The Gold Study and Project submission ID number in Joint Genome Institute IMG/M for the metagenome is Gs0047444 and Gp0055765.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01845/fulloil sandstailings pondhydrocarbon degradationbenzenenaphthalenemetagenomics
collection DOAJ
language English
format Article
sources DOAJ
author Fauziah F. Rochman
Andriy Sheremet
Ivica Tamas
Ivica Tamas
Alireza Saidi-Mehrabad
Alireza Saidi-Mehrabad
Joong-Jae Kim
Xiaoli Dong
Xiaoli Dong
Christoph W. Sensen
Christoph W. Sensen
Lisa M. Gieg
Peter F. Dunfield
spellingShingle Fauziah F. Rochman
Andriy Sheremet
Ivica Tamas
Ivica Tamas
Alireza Saidi-Mehrabad
Alireza Saidi-Mehrabad
Joong-Jae Kim
Xiaoli Dong
Xiaoli Dong
Christoph W. Sensen
Christoph W. Sensen
Lisa M. Gieg
Peter F. Dunfield
Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
Frontiers in Microbiology
oil sands
tailings pond
hydrocarbon degradation
benzene
naphthalene
metagenomics
author_facet Fauziah F. Rochman
Andriy Sheremet
Ivica Tamas
Ivica Tamas
Alireza Saidi-Mehrabad
Alireza Saidi-Mehrabad
Joong-Jae Kim
Xiaoli Dong
Xiaoli Dong
Christoph W. Sensen
Christoph W. Sensen
Lisa M. Gieg
Peter F. Dunfield
author_sort Fauziah F. Rochman
title Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
title_short Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
title_full Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
title_fullStr Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
title_full_unstemmed Benzene and Naphthalene Degrading Bacterial Communities in an Oil Sands Tailings Pond
title_sort benzene and naphthalene degrading bacterial communities in an oil sands tailings pond
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-09-01
description Oil sands process-affected water (OSPW), produced by surface-mining of oil sands in Canada, is alkaline and contains high concentrations of salts, metals, naphthenic acids, and polycyclic aromatic compounds (PAHs). Residual hydrocarbon biodegradation occurs naturally, but little is known about the hydrocarbon-degrading microbial communities present in OSPW. In this study, aerobic oxidation of benzene and naphthalene in the surface layer of an oil sands tailings pond were measured. The potential oxidation rates were 4.3 μmol L−1 OSPW d−1 for benzene and 21.4 μmol L−1 OSPW d−1 for naphthalene. To identify benzene and naphthalene-degrading microbial communities, metagenomics was combined with stable isotope probing (SIP), high-throughput sequencing of 16S rRNA gene amplicons, and isolation of microbial strains. SIP using 13C-benzene and 13C-naphthalene detected strains of the genera Methyloversatilis and Zavarzinia as the main benzene degraders, while strains belonging to the family Chromatiaceae and the genus Thauera were the main naphthalene degraders. Metagenomic analysis revealed a diversity of genes encoding oxygenases active against aromatic compounds. Although these genes apparently belonged to many phylogenetically diverse taxa, only a few of these taxa were predominant in the SIP experiments. This suggested that many members of the community are adapted to consuming other aromatic compounds, or are active only under specific conditions. 16S rRNA gene sequence datasets have been submitted to the Sequence Read Archive (SRA) under accession number SRP109130. The Gold Study and Project submission ID number in Joint Genome Institute IMG/M for the metagenome is Gs0047444 and Gp0055765.
topic oil sands
tailings pond
hydrocarbon degradation
benzene
naphthalene
metagenomics
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01845/full
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