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

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.

Hydrocarbon degraders establish at the costs of microbial richness, abundance and keystone taxa after crude oil contamination in permafrost environments

“…This genus comprises known plant symbionts and nitrogen-fixing bacteria, and more recently some have been reported as capable to degrade PAHs4647. Furthermore, genomic analysis showed that some species of Rhizobium , Bradyrhizobium and Mesorhizobium additionally harbour multiple genes for acyl-homoserine lactone (AHL) or autoinducer (AI) quorum-sensing (QS) molecules, which may suggest that bacterial hydrocarbon degradation is a QS-regulated process4648.…”

“…Furthermore, genomic analysis showed that some species of Rhizobium , Bradyrhizobium and Mesorhizobium additionally harbour multiple genes for acyl-homoserine lactone (AHL) or autoinducer (AI) quorum-sensing (QS) molecules, which may suggest that bacterial hydrocarbon degradation is a QS-regulated process4648. Several studies have demonstrated that degradation of environmental contaminants is enhanced in the plant rhizosphere4749 and inoculation with Rhizobium melitoti was reported to specifically stimulate the growth and activity of indigenous hydrocarbon-degrading microorganisms50. In the light of these observations, our data further support the concept that increased selection pressure due to exposure to contaminants stimulates communication and cooperation amongst members of the permafrost microbial community, especially in the upper active layer.…”

Evaluation of the use of legumes for biodegradation of petroleum hydrocarbons in soil

“…Similar reason could also be deduced for other legumes species in which only 2.77 and 6.46% concentration of the fraction was recovered from the residual oil extracted from A. hypogea and M. sativa, respectively. This is not surprising as many authors reported that the enhancement of specific organisms may lead to the preferential degradation of either aliphatics or aromatics, with degradation of the remaining class of compounds being inhibited as a result of catabolite repression (Rentz et al 2004;Phillips 2008;Martin et al 2014;Pagé et al 2015).…”

Rhizoremediation of petroleum hydrocarbons: a model system for plant microbiome manipulation

“…For instance, in a pot study, transcripts related to Alphaproteobacteria , Betaproteobacteria , Gammaproteobacteria and Acidobacteria were more abundant in the rhizosphere of willows growing in contaminated soil as compared to non‐contaminated soils (Yergeau et al ., ). Also, functional genes related to aromatic and aliphatic hydrocarbon degradation were more prevalent in the rhizosphere of willows growing in contaminated soils (Yergeau et al ., ), and these genes were shown to be related to bacterial orders such as Actinomycetales , Rhodospirillales , Burkholderiales , Alteromonadales , Solirubrobacterales , Caulobacterales and Rhizobiales (Pagé et al ., ). In the field, the differences in the expression of hydrocarbon degradation genes and in the active taxa between the rhizosphere of willows growing in contaminated and non‐con‐taminated soils varied and depended on the willow species (Yergeau et al ., ).…”

“…Generally, indigenous hydrocarbon‐degrading microbes in contaminated soils can be efficiently stimulated by plants (Yergeau et al ., ; Pagé et al ., ) or fertilizers (Yergeau et al ., , ; Bell et al ., ). Bioaugmentation (inoculations) with a single or a few hydrocarbon‐degrading strains is thus generally ineffective (Thomassin‐Lacroix et al ., ), and it has been shown that pre‐selecting microorganisms that can degrade hydrocarbons results in less efficient degradation than using the entirety of the microbes present in a soil (Bell et al ., ).…”