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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 enhances natural microbial degradation. However, little is known about how different initial microbiotas influence the rhizodegradation outcome. Recent studies have hinted that soil initial diversity has a determining effect on the outcome of contaminant degradation. To test this, we either 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 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 abundances 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 hydrocarbons (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 harnessing the potential of phytoremediation. Therefore, this study focused on determining the effect of two different soil types in the fate of phenanthrene (a polycyclic aromatic hydrocarbon) under balsam poplar remediation. Poplar increased the degradation of phenanthrene in forest, but not in agricultural soil. The fungi were affected by poplars, whereas total bacteria and specific PAH-degrading bacteria 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.

SUBMITTER: Correa-Garcia S

PROVIDER: S-EPMC7783334 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The anthropogenic release of oil hydrocarbons into the cold marine environment is an increasing concern due to the elevated usage of sea routes and the exploration of new oil drilling sites in Arctic areas. The aim of this study was to evaluate prokaryotic community structures and the genetic potential of hydrocarbon degradation in the metagenomes of seawater, sea ice, and crude oil encapsulating the sea ice of the Norwegian fjord, Ofotfjorden. Although the results indicated substantial differences between the structure of prokaryotic communities in seawater and sea ice, the crude oil encapsulating sea ice (SIO) showed increased abundances of many genera-containing hydrocarbon-degrading organisms, including Bermanella, Colwellia, and Glaciecola. Although the metagenome of seawater was rich in a variety of hydrocarbon degradation-related functional genes (HDGs) associated with the metabolism of n-alkanes, and mono- and polyaromatic hydrocarbons, most of the normalized gene counts were highest in the clean sea ice metagenome, whereas in SIO, these counts were the lowest. The long-chain alkane degradation gene almA was detected from all the studied metagenomes and its counts exceeded ladA and alkB counts in both sea ice metagenomes. In addition, almA was related to the most diverse group of prokaryotic genera. Almost all 18 good- and high-quality metagenome-assembled genomes (MAGs) had diverse HDGs profiles. The MAGs recovered from the SIO metagenome belonged to the abundant taxa, such as Glaciecola, Bermanella, and Rhodobacteracea, in this environment. The genera associated with HDGs were often previously known as hydrocarbon-degrading genera. However, a substantial number of new associations, either between already known hydrocarbon-degrading genera and new HDGs or between genera not known to contain hydrocarbon degraders and multiple HDGs, were found. The superimposition of the results of comparing HDG associations with taxonomy, the HDG profiles of MAGs, and the full genomes of organisms in the KEGG database suggest that the found relationships need further investigation and verification.

Project description:UNLABELLED: Understanding the interactions among different species and their responses to environmental changes, such as elevated atmospheric concentrations of CO(2), is a central goal in ecology but is poorly understood in microbial ecology. Here we describe a novel random matrix theory (RMT)-based conceptual framework to discern phylogenetic molecular ecological networks using metagenomic sequencing data of 16S rRNA genes from grassland soil microbial communities, which were sampled from a long-term free-air CO(2) enrichment experimental facility at the Cedar Creek Ecosystem Science Reserve in Minnesota. Our experimental results demonstrated that an RMT-based network approach is very useful in delineating phylogenetic molecular ecological networks of microbial communities based on high-throughput metagenomic sequencing data. The structure of the identified networks under ambient and elevated CO(2) levels was substantially different in terms of overall network topology, network composition, node overlap, module preservation, module-based higher-order organization, topological roles of individual nodes, and network hubs, suggesting that the network interactions among different phylogenetic groups/populations were markedly changed. Also, the changes in network structure were significantly correlated with soil carbon and nitrogen contents, indicating the potential importance of network interactions in ecosystem functioning. In addition, based on network topology, microbial populations potentially most important to community structure and ecosystem functioning can be discerned. The novel approach described in this study is important not only for research on biodiversity, microbial ecology, and systems microbiology but also for microbial community studies in human health, global change, and environmental management. IMPORTANCE: The interactions among different microbial populations in a community play critical roles in determining ecosystem functioning, but very little is known about the network interactions in a microbial community, owing to the lack of appropriate experimental data and computational analytic tools. High-throughput metagenomic technologies can rapidly produce a massive amount of data, but one of the greatest difficulties is deciding how to extract, analyze, synthesize, and transform such a vast amount of information into biological knowledge. This study provides a novel conceptual framework to identify microbial interactions and key populations based on high-throughput metagenomic sequencing data. This study is among the first to document that the network interactions among different phylogenetic populations in soil microbial communities were substantially changed by a global change such as an elevated CO(2) level. The framework developed will allow microbiologists to address research questions which could not be approached previously, and hence, it could represent a new direction in microbial ecology research.

Project description:ObjectiveThe potential ecological risk index (RI) is the most commonly used method to assess heavy metals (HMs) contamination in soils. However, studies have focused on the response of soil microorganisms to different concentrations, whereas little is known about the responses of the microbial community structures and functions to HMs at different RI levels.MethodsHere, we conducted soil microcosms with low (L), medium (M) and high (H) RI levels, depending on the Pb and Cd concentrations, were conducted. The original soil was used as the control (CK). High-throughput sequencing, qPCR, and Biolog plate approaches were applied to investigate the microbial community structures, abundance, diversity, metabolic capacity, functional genes, and community assembly processes.ResultThe abundance and alpha diversity indices for the bacteria at different RI levels were significantly lower than those of the CK. Meanwhile, the abundance and ACE index for the fungi increased significantly with RI levels. Acidobacteria, Basidiomycota and Planctomycetes were enriched as the RI level increased. Keystone taxa and co-occurrence pattern analysis showed that rare taxa play a vital role in the stability and function of the microbial community at different RI levels. Network analysis indicates that not only did the complexity and vulnerability of microbial community decrease as risk levels increased, but that the lowest number of keystone taxa was found at the H level. However, the microbial community showed enhanced intraspecific cooperation to adapt to the HMs stress. The Biolog plate data suggested that the average well color development (AWCD) reduced significantly with RI levels in bacteria, whereas the fungal AWCD was dramatically reduced only at the H level. The functional diversity indices and gene abundance for the microorganisms at the H level were significantly lower than those the CK. In addition, microbial community assembly tended to be more stochastic with an increase in RI levels.ConclusionOur results provide new insight into the ecological impacts of HMs on the soil microbiome at different risk levels, and will aid in future risk assessments for Pb and Cd contamination.

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

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