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      Salix purpurea Stimulates the Expression of Specific Bacterial Xenobiotic Degradation Genes in a Soil Contaminated with Hydrocarbons

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      PLoS ONE
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          Abstract

          The objectives of this study were to uncover Salix purpurea-microbe xenobiotic degradation systems that could be harnessed in rhizoremediation, and to identify microorganisms that are likely involved in these partnerships. To do so, we tested S. purpurea‘s ability to stimulate the expression of 10 marker microbial oxygenase genes in a soil contaminated with hydrocarbons. In what appeared to be a detoxification rhizosphere effect, transcripts encoding for alkane 1-monooxygenases, cytochrome P450 monooxygenases, laccase/polyphenol oxidases, and biphenyl 2,3-dioxygenase small subunits were significantly more abundant in the vicinity of the plant's roots than in bulk soil. This gene expression induction is consistent with willows' known rhizoremediation capabilities, and suggests the existence of S. purpurea-microbe systems that target many organic contaminants of interest (i.e. C4-C16 alkanes, fluoranthene, anthracene, benzo(a)pyrene, biphenyl, polychlorinated biphenyls). An enhanced expression of the 4 genes was also observed within the bacterial orders Actinomycetales, Rhodospirillales, Burkholderiales, Alteromonadales, Solirubrobacterales, Caulobacterales, and Rhizobiales, which suggest that members of these taxa are active participants in the exposed partnerships. Although the expression of the other 6 marker genes did not appear to be stimulated by the plant at the community level, signs of additional systems that rest on their expression by members of the orders Solirubrobacterales, Sphingomonadales, Actinomycetales, and Sphingobacteriales were observed. Our study presents the first transcriptomics-based identification of microbes whose xenobiotic degradation activity in soil appears stimulated by a plant. It paints a portrait that contrasts with the current views on these consortia's composition, and opens the door for the development of laboratory test models geared towards the identification of root exudate characteristics that limit the efficiency of current willow-based rhizoremediation applications.

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          Most cited references35

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          Root exudation and rhizosphere biology.

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            Using soil bacteria to facilitate phytoremediation.

            In the past twenty years or so, researchers have endeavored to utilize plants to facilitate the removal of both organic and inorganic contaminants from the environment, especially from soil. These phytoremediation approaches have come a long way in a short time. However, the majority of this work has been done under more controlled laboratory conditions and not in the field. As an adjunct to various phytoremediation strategies and as part of an effort to make this technology more efficacious, a number of scientists have begun to explore the possibility of using various soil bacteria together with plants. These bacteria include biodegradative bacteria, plant growth-promoting bacteria and bacteria that facilitate phytoremediation by other means. An overview of bacterially assisted phytoremediation is provided here for both organic and metallic contaminants, with the intent of providing some insight into how these bacteria aid phytoremediation so that future field studies might be facilitated. (c) 2010 Elsevier Inc. All rights reserved.
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              Degradation of alkanes by bacteria.

              Pollution of soil and water environments by crude oil has been, and is still today, an important problem. Crude oil is a complex mixture of thousands of compounds. Among them, alkanes constitute the major fraction. Alkanes are saturated hydrocarbons of different sizes and structures. Although they are chemically very inert, most of them can be efficiently degraded by several microorganisms. This review summarizes current knowledge on how microorganisms degrade alkanes, focusing on the biochemical pathways used and on how the expression of pathway genes is regulated and integrated within cell physiology.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                10 July 2015
                2015
                : 10
                : 7
                : e0132062
                Affiliations
                [1 ]Department of Natural Resource Sciences, McGill University, Montréal, Québec, Canada
                [2 ]Energy, Mining and Environment, National Research Council Canada, Montréal, Québec, Canada
                NERC Centre for Ecology & Hydrology, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: APP EY CWG. Performed the experiments: APP EY CWG. Analyzed the data: APP EY. Contributed reagents/materials/analysis tools: APP EY CWG. Wrote the paper: APP EY CWG.

                Article
                PONE-D-15-08845
                10.1371/journal.pone.0132062
                4498887
                26161539
                c0111235-0463-4e4a-bfc7-f51958a69062
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 2 March 2015
                : 9 June 2015
                Page count
                Figures: 3, Tables: 2, Pages: 16
                Funding
                Genome Canada/Génome Québec Grant 2510 ( www.genomecanada.ca) ( www.genomequebec.com). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Messenger RNA datasets associated with the 12 metatranscriptomes are publicly available on the MG-RAST website ( https://metagenomics.anl.gov/, IDs 4512575-4512580 for bulk soil and 4512587-4512592 for rhizosphere soil) ( http://metagenomics.anl.gov/?page=MetagenomeProject&project=3266).

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