Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study

Bioremediation offers a sustainable approach for removal of polycyclic aromatic hydrocarbons (PAHs) from the environment; however, information regarding the microbial communities involved remains limited. In this study, microbial community dynamics and the abundance of the key gene (PAH-RHDα) encodi...

Full description

Bibliographic Details
Main Authors: Sean Storey, Mardiana Mohd Ashaari, Nicholas Clipson, Evelyn Doyle, Alexandre B. de Menezes
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02815/full
id doaj-5211f05bc4054f228a61b8d4dbdaeff9
record_format Article
spelling doaj-5211f05bc4054f228a61b8d4dbdaeff92020-11-24T21:47:11ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-11-01910.3389/fmicb.2018.02815339359Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based StudySean Storey0Sean Storey1Mardiana Mohd Ashaari2Nicholas Clipson3Nicholas Clipson4Evelyn Doyle5Evelyn Doyle6Alexandre B. de Menezes7School of Biology and Environmental Science, University College Dublin, Dublin, IrelandEarth Institute, University College Dublin, Dublin, IrelandDepartment of Biotechnology, Kulliyah of Science, International Islamic University Malaysia, Malaysia, MalaysiaSchool of Biology and Environmental Science, University College Dublin, Dublin, IrelandEarth Institute, University College Dublin, Dublin, IrelandSchool of Biology and Environmental Science, University College Dublin, Dublin, IrelandEarth Institute, University College Dublin, Dublin, IrelandMicrobiology, School of Natural Sciences, Ryan Institute, National University of Ireland, Galway, IrelandBioremediation offers a sustainable approach for removal of polycyclic aromatic hydrocarbons (PAHs) from the environment; however, information regarding the microbial communities involved remains limited. In this study, microbial community dynamics and the abundance of the key gene (PAH-RHDα) encoding a ring hydroxylating dioxygenase involved in PAH degradation were examined during degradation of phenanthrene in a podzolic soil from the site of a former timber treatment facility. The 10,000-fold greater abundance of this gene associated with Gram-positive bacteria found in phenanthrene-amended soil compared to unamended soil indicated the likely role of Gram-positive bacteria in PAH degradation. In contrast, the abundance of the Gram-negative PAHs-RHDα gene was very low throughout the experiment. While phenanthrene induced increases in the abundance of a small number of OTUs from the Actinomycetales and Sphingomonadale, most of the remainder of the community remained stable. A single unclassified OTU from the Micrococcaceae family increased ~20-fold in relative abundance, reaching 32% of the total sequences in amended microcosms on day 7 of the experiment. The relative abundance of this same OTU increased 4.5-fold in unamended soils, and a similar pattern was observed for the second most abundant PAH-responsive OTU, classified into the Sphingomonas genus. Furthermore, the relative abundance of both of these OTUs decreased substantially between days 7 and 17 in the phenanthrene-amended and control microcosms. This suggests that their opportunistic phenotype, in addition to likely PAH-degrading ability, was determinant in the vigorous growth of dominant PAH-responsive OTUs following phenanthrene amendment. This study provides new information on the temporal response of soil microbial communities to the presence and degradation of a significant environmental pollutant, and as such has the potential to inform the design of PAH bioremediation protocols.https://www.frontiersin.org/article/10.3389/fmicb.2018.02815/fullpolycyclic aromatic hydrocarbonsmicrobiomebioremediationsoilphenanthrene
collection DOAJ
language English
format Article
sources DOAJ
author Sean Storey
Sean Storey
Mardiana Mohd Ashaari
Nicholas Clipson
Nicholas Clipson
Evelyn Doyle
Evelyn Doyle
Alexandre B. de Menezes
spellingShingle Sean Storey
Sean Storey
Mardiana Mohd Ashaari
Nicholas Clipson
Nicholas Clipson
Evelyn Doyle
Evelyn Doyle
Alexandre B. de Menezes
Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
Frontiers in Microbiology
polycyclic aromatic hydrocarbons
microbiome
bioremediation
soil
phenanthrene
author_facet Sean Storey
Sean Storey
Mardiana Mohd Ashaari
Nicholas Clipson
Nicholas Clipson
Evelyn Doyle
Evelyn Doyle
Alexandre B. de Menezes
author_sort Sean Storey
title Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
title_short Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
title_full Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
title_fullStr Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
title_full_unstemmed Opportunistic Bacteria Dominate the Soil Microbiome Response to Phenanthrene in a Microcosm-Based Study
title_sort opportunistic bacteria dominate the soil microbiome response to phenanthrene in a microcosm-based study
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-11-01
description Bioremediation offers a sustainable approach for removal of polycyclic aromatic hydrocarbons (PAHs) from the environment; however, information regarding the microbial communities involved remains limited. In this study, microbial community dynamics and the abundance of the key gene (PAH-RHDα) encoding a ring hydroxylating dioxygenase involved in PAH degradation were examined during degradation of phenanthrene in a podzolic soil from the site of a former timber treatment facility. The 10,000-fold greater abundance of this gene associated with Gram-positive bacteria found in phenanthrene-amended soil compared to unamended soil indicated the likely role of Gram-positive bacteria in PAH degradation. In contrast, the abundance of the Gram-negative PAHs-RHDα gene was very low throughout the experiment. While phenanthrene induced increases in the abundance of a small number of OTUs from the Actinomycetales and Sphingomonadale, most of the remainder of the community remained stable. A single unclassified OTU from the Micrococcaceae family increased ~20-fold in relative abundance, reaching 32% of the total sequences in amended microcosms on day 7 of the experiment. The relative abundance of this same OTU increased 4.5-fold in unamended soils, and a similar pattern was observed for the second most abundant PAH-responsive OTU, classified into the Sphingomonas genus. Furthermore, the relative abundance of both of these OTUs decreased substantially between days 7 and 17 in the phenanthrene-amended and control microcosms. This suggests that their opportunistic phenotype, in addition to likely PAH-degrading ability, was determinant in the vigorous growth of dominant PAH-responsive OTUs following phenanthrene amendment. This study provides new information on the temporal response of soil microbial communities to the presence and degradation of a significant environmental pollutant, and as such has the potential to inform the design of PAH bioremediation protocols.
topic polycyclic aromatic hydrocarbons
microbiome
bioremediation
soil
phenanthrene
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02815/full
work_keys_str_mv AT seanstorey opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT seanstorey opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT mardianamohdashaari opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT nicholasclipson opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT nicholasclipson opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT evelyndoyle opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT evelyndoyle opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
AT alexandrebdemenezes opportunisticbacteriadominatethesoilmicrobiomeresponsetophenanthreneinamicrocosmbasedstudy
_version_ 1725898909406986240