Soil Characteristics Constrain the Response of Microbial Communities and Associated Hydrocarbon Degradation Genes during Phytoremediation

Abstract

Rhizodegradation is a promising cleanup technology where microorganisms degrade soil contaminants in the rhizosphere. A symbiotic relationship is expected to occur between plant roots and soil microorganisms in contaminated soils that enhance natural microbial degradation in soils. However, little is known about how this initial microbiota influences the rhizodegradation outcome in a context of different soil microbiotas. Recent studies have hinted that soil initial diversity has a determining effect on the outcome of contaminant degradation. To test this, we planted (P) or not (NP) balsam poplars (Populus balsamifera) in two soils of contrasting diversity (agricultural and forest) that were contaminated or not with 50 mg kg-1 of phenanthrene (PHE). The DNA from the rhizosphere of the P and the bulk soil of the NP pots was extracted and the bacterial genes encoding for the 16S rRNA, the PAH ring-hydroxylating dioxygenase alpha subunits (PAH-RHDα) of gram-positive and gram-negative bacteria, and the fungal ITS region were sequenced to characterize the microbial communities. The abundance of the PAH-RHDα genes were quantified by real-time quantitative PCR. Plant presence had a significant effect on PHE degradation only in the forest soil, whereas both NP and P agricultural soils degraded the same amount of PHE. Fungal communities were mainly affected by plant presence, whereas bacterial communities were principally affected by the soil type, and upon contamination the dominant PAH degrading community was similarly constrained by soil type. Our results highlight the crucial importance of soil microbial and physicochemical characteristics in the outcome of rhizoremediation. IMPORTANCE Polycyclic aromatic hydrocarbon (PAH) are a group of organic contaminants that pose a risk to ecosystems' health. Phytoremediation is a promising biotechnology with the potential to restore PAH contaminated soils. However, some limitations prevent it from becoming the remediation technology of reference, despite being environmentally friendlier than mainstream physicochemical alternatives. Recent reports suggest that the original soil microbial diversity is the key to harness the potential of phytoremediation. Therefore, this study focused on determining the effect of two different soil types in the fate of phenanthrene under balsam poplar remediation. Poplar increased the degradation of phenanthrene in forest, but not in agricultural soil. The fungi were affected by poplars, whereas bacteria and PAH degraders were constrained by soil type, leading to different degradation patterns between soils. These results highlight the importance of performing preliminary microbiological studies of contaminated soils to determine whether plant presence could improve remediation rates or not.

Animal soil food web complexity triggers shifts in microbial communities, including PAH degraders, but without clear effects on phenanthrene phytoremediation

“…The phenanthrene contamination triggered a general reduction of the fungal diversity, which was driven by large increases in the relative abundance of Sphaerosporella. The predominance of this fungus has already been reported in other pot and field phytoremediation experiments carried out with trees (Bell et al, 2014a;Correa-García et al, 2021;Dagher et al, 2020;Danielson, 2007;Yergeau et al, 2015). Furthermore, its presence in the rhizosphere or in the bulk soil of pots with tree cuttings has been related to an enhancement of plant biomass (Yergeau et al, 2015) and to resistance to contamination stress (Bell et al, 2014a), probably through its role as an ectomycorrhiza (Danielson, 2007).…”

“…Plant height and the number of shoots were measured prior to clipping aboveground shoot biomass (excluding the original cutting). Afterwards, the cuttings with the attached roots were taken out from the pots and rhizosphere and bulk soil samples were collected for microbial community analysis and phenanthrene concentration measurements as described in Correa-García et al, (2021), resulting in 192 soil samples. Soil samples were kept at 4 C until transportation to the lab (around 2 h) where they were placed at -20 C.…”

“…The DNA isolation steps and the library preparation follow the steps described in-depth in Correa-García et al, (2021). Briefly, 250 mg per sample of bulk or rhizosphere soil were transferred to a 2 mL Powerbead Pro tube.…”

Microbiological Study in Petrol-Spiked Soil

“…According to Ite and Ibok [ 53 ], the effectiveness of biodegradability of oil components is as follows: n-alkanes > branched alkenes > low molecular weight n-alkyl aromatics > monoaromatics > cyclic alkanes > polycyclic aromatic hydrocarbons > asphaltene. Degradation of hydrocarbons in the soil is strongly associated with root secretions that ensure the rhizodegradation of organic pollutants [ 85 , 86 , 87 ].…”

Elucidating the Rhizosphere Associated Bacteria for Environmental Sustainability

“…Some bacterial species have synergistic interactions (direct or indirect) with environmental factors capable of removing hydrocarbon and heavy metal pollutants from soils, which consequently successfully increases the movement of these pollutants to the above-ground plants' biomass. Rhizoremediation, a phytoremediation approach, is plant-microbe cooperation with the potential to remove soil pollutants through the action of microorganisms and plant enzymes in the rhizosphere [97].…”