Dataset Information

Manure Application Did Not Enrich Antibiotic Resistance Genes in Root Endophytic Bacterial Microbiota of Cherry Radish Plants.

ABSTRACT: Growing evidence suggests that livestock manure used as organic fertilizer in agriculture may lead to the potential propagation of antibiotic resistance genes (ARGs) from "farm to fork." However, little is known about the impacts of manure fertilization on the incidence of ARGs in the plant-associated microbiomes (including rhizosphere, endosphere, and phyllosphere), which hampers our ability to assess the dissemination of antibiotic resistance in the soil-plant system. Here, we constructed a pot experiment to explore the effects of poultry and cattle manure applications on the shifts in the resistome in the plant microbiome of harvested cherry radish. A total of 144 ARGs conferring resistance to eight major classes of antibiotics were detected among all the samples. Rhizosphere and phyllosphere microbiomes harbored significantly higher diversity and abundance of ARGs than did root endophytic microbiomes of cherry radish. Manure application significantly increased the abundance of ARGs in the rhizosphere and phyllosphere but not in the endophytes of the root, which is the edible part of cherry radish. Soil and plant microbiomes changed dramatically after manure applications and clustered separately according to different sample types and treatments. Structural equation modeling revealed that bacterial abundance was the most important factor modulating the distribution patterns of soil and plant resistomes after accounting for multiple drivers. Taken together, we provide evidence that enrichment of the resistome in the rhizosphere and phyllosphere of cherry radish is more obvious than with the endosphere after manure application, suggesting that manure amendment might not enhance the dissemination of ARGs into the root of vegetables in the pot experiment.IMPORTANCE Our study provides important evidence that manure application increased the occurrence of ARGs in the rhizosphere and phyllosphere of cherry radish, compared with that in the endophytic bacterial microbiota of root, which is the edible part of cherry radish. Our findings suggest that although manure amendment is a significant route of ARGs entering agricultural soils, these manure-derived ARGs may be at low risk of migrating into the endophytes of root vegetables.

SUBMITTER: Zhang YJ

PROVIDER: S-EPMC6952223 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Manure Application Did Not Enrich Antibiotic Resistance Genes in Root Endophytic Bacterial Microbiota of Cherry Radish Plants.

Zhang Yu-Jing YJ Hu Hang-Wei HW Chen Qing-Lin QL Yan Hui H Wang Jun-Tao JT Chen Deli D He Ji-Zheng JZ

Applied and environmental microbiology 20200107 2

Growing evidence suggests that livestock manure used as organic fertilizer in agriculture may lead to the potential propagation of antibiotic resistance genes (ARGs) from "farm to fork." However, little is known about the impacts of manure fertilization on the incidence of ARGs in the plant-associated microbiomes (including rhizosphere, endosphere, and phyllosphere), which hampers our ability to assess the dissemination of antibiotic resistance in the soil-plant system. Here, we constructed a po ...[more]

PMID: 31704674

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Project description:The plant microbiome plays a critical role in plant growth, development, and health, with endophytes being recognized as essential members due to their close interactions with host plants. However, knowledge gaps remain in understanding the mechanisms driving the colonization and establishment of endophytic communities. To address this issue, we investigated the microbiota of tobacco roots and leaves, including both epiphytic and endophytic microorganisms. We found that Actinobacteria and Alphaproteobacteria were significantly enriched in the root endosphere. Additionally, we identified higher abundances of functional traits involved in antibiotic synthesis, plant cell wall degradation, iron metabolism, secretion systems, and nicotine degradation enzymes in the endosphere. We further studied metagenome-assembled genomes from the rhizosphere and root endosphere, revealing a greater diversity of secondary metabolites in bacteria within the root endosphere. Together, this study provides insights into the taxonomic and functional assembly cues that may contribute to shaping the endophytic plant microbiota.IMPORTANCEThe presence of diverse microorganisms within plant tissues under natural conditions is a well-established fact. However, due to the plant immune system's barrier and the unique microhabitat of the plant interior, it remains unclear what specific characteristics bacteria require to successfully colonize and thrive in the plant endosphere. Recognizing the significance of unraveling these functional features, our study focused on investigating the enriched traits in the endophytic microbiota compared to the epiphytes. Through our research, we have successfully identified the taxonomic and functional assembly cues that drive the enrichment of the endophytic microbiota across the epiphytic compartments. These findings shed new light on the intricate mechanisms of endophyte colonization, thereby deepening our understanding of plant-microbe interactions and paving the way for further advancements in microbiome manipulation.

Project description:Dairy cattle are routinely treated with antibiotics, and the resulting manure or composted manure is commonly used as a soil amendment for crop production, raising questions regarding the potential for antibiotic resistance to propagate from "farm to fork." The objective of this study was to compare the microbiota and "resistomes" (i.e., carriage of antibiotic resistance genes [ARGs]) associated with lettuce leaf and radish taproot surfaces grown in different soils amended with dairy manure, compost, or chemical fertilizer only (control). Manure was collected from antibiotic-free dairy cattle (DC) or antibiotic-treated dairy cattle (DA), with a portion composted for parallel comparison. Amendments were applied to loamy sand or silty clay loam, and lettuce and radishes were cultivated to maturity in a greenhouse. Metagenomes were profiled via shotgun Illumina sequencing. Radishes carried a distinct ARG composition compared to that of lettuce, with greater relative abundance of total ARGs. Taxonomic species richness was also greater for radishes by 1.5-fold. The resistomes of lettuce grown with DC compost were distinct from those grown with DA compost, DC manure, or fertilizer only. Further, compost applied to loamy sand resulted in twofold-greater relative abundance of total ARGs on lettuce than when applied to silty clay loam. The resistomes of radishes grown with biological amendments were distinct from the corresponding fertilizer controls, but effects of composting or antibiotic use were not measureable. Cultivation in loamy sand resulted in higher species richness for both lettuce and radishes than when grown in silty clay loam by 2.2-fold and 1.2-fold, respectively, when amended with compost.IMPORTANCE A controlled, integrated, and replicated greenhouse study, along with comprehensive metagenomic analysis, revealed that multiple preharvest factors, including antibiotic use during manure collection, composting, biological soil amendment, and soil type, influence vegetable-borne resistomes. Here, radishes, a root vegetable, carried a greater load of ARGs and species richness than lettuce, a leafy vegetable. However, the lettuce resistome was more noticeably influenced by upstream antibiotic use and composting. Network analysis indicated that cooccurring ARGs and mobile genetic elements were almost exclusively associated with conditions receiving raw manure amendments, suggesting that composting could alleviate the mobility of manure-derived resistance traits. Effects of preharvest factors on associated microbiota and resistomes of vegetables eaten raw are worthy of further examination in terms of potential influence on human microbiomes and spread of antibiotic resistance. This research takes a step toward identifying on-farm management practices that can help mitigate the spread of agricultural sources of antibiotic resistance.

Dataset Information

Manure Application Did Not Enrich Antibiotic Resistance Genes in Root Endophytic Bacterial Microbiota of Cherry Radish Plants.

Publications

Manure Application Did Not Enrich Antibiotic Resistance Genes in Root Endophytic Bacterial Microbiota of Cherry Radish Plants.

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