Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments

Qian Xiang, Dong Zhu, Madeline Giles, Roy Neilson, Xiao-Ru Yang, Min Qiao, Qing-Lin Chen (Lead / Corresponding author)

Research output: Contribution to journalArticle

Abstract

The plant microbiome represents a crucial pathway for human exposure to environmental antibiotic resistance. However, little information is available regarding the plant associated resistome in human-related environments at a larger scale. Here, by high-throughput quantitative-PCR chip-based array and amplicon sequencing, we characterized antibiotic resistance genes (ARGs) and bacterial communities in plant and soil microbiomes from human highly disturbed peri-urban farmland and less disturbed forest at a watershed scale. A total of 71 ARGs were detected in the phyllosphere, which covered almost all the major recognized classes of antibiotics that are administered commonly to humans and animals. The overall pattern of the plant associated resistome in intensive anthropogenic influenced farmland was significantly different from that of forest environments (PERMANOVA, P < 0.01), indicating that agricultural activities might be important drivers in shaping the plant resistome. A bipartite network analysis suggested that all ARGs detected in the plant microbiome were also present in the soil microbiome. Together, our findings provide a better understanding of the plant resistome and suggest that land use is a key contributor to the composition of ARG profiles in the plant phyllosphere, and that the soil resistome may represent a critical reservoir of plant associated ARGs.

Original languageEnglish
Article number121068
Pages (from-to)1-8
Number of pages8
JournalJournal of Hazardous Materials
Volume382
Early online date21 Aug 2019
DOIs
Publication statusE-pub ahead of print - 21 Aug 2019

Fingerprint

phyllosphere
Microbiota
Antibiotics
antibiotic resistance
Anti-Bacterial Agents
Microbial Drug Resistance
Genes
gene
Soils
Soil
agricultural land
Bacterial Drug Resistance
Electric network analysis
Watersheds
Land use
soil
network analysis
Environmental Exposure
Animals
antibiotics

Cite this

Xiang, Qian ; Zhu, Dong ; Giles, Madeline ; Neilson, Roy ; Yang, Xiao-Ru ; Qiao, Min ; Chen, Qing-Lin. / Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments. In: Journal of Hazardous Materials. 2020 ; Vol. 382. pp. 1-8.
@article{98cd6486c54e4a1e8faa735a317e03c8,
title = "Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments",
abstract = "The plant microbiome represents a crucial pathway for human exposure to environmental antibiotic resistance. However, little information is available regarding the plant associated resistome in human-related environments at a larger scale. Here, by high-throughput quantitative-PCR chip-based array and amplicon sequencing, we characterized antibiotic resistance genes (ARGs) and bacterial communities in plant and soil microbiomes from human highly disturbed peri-urban farmland and less disturbed forest at a watershed scale. A total of 71 ARGs were detected in the phyllosphere, which covered almost all the major recognized classes of antibiotics that are administered commonly to humans and animals. The overall pattern of the plant associated resistome in intensive anthropogenic influenced farmland was significantly different from that of forest environments (PERMANOVA, P < 0.01), indicating that agricultural activities might be important drivers in shaping the plant resistome. A bipartite network analysis suggested that all ARGs detected in the plant microbiome were also present in the soil microbiome. Together, our findings provide a better understanding of the plant resistome and suggest that land use is a key contributor to the composition of ARG profiles in the plant phyllosphere, and that the soil resistome may represent a critical reservoir of plant associated ARGs.",
author = "Qian Xiang and Dong Zhu and Madeline Giles and Roy Neilson and Xiao-Ru Yang and Min Qiao and Qing-Lin Chen",
note = "This research was funded by the National Key Research and Development Program of China (2017YFE0107300), Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020402), Water Science and Technology Fund of Jiangxi Province in China (KT201702) and the Natural Environment Research Council (NE/N00745X/1 and NE/S009132). The James Hutton Institute receives financial support from the Scottish Government Rural and Environment Science and Analytical Services Division. Copyright {\circledC} 2019 Elsevier B.V. All rights reserved.",
year = "2019",
month = "8",
day = "21",
doi = "10.1016/j.jhazmat.2019.121068",
language = "English",
volume = "382",
pages = "1--8",
journal = "Journal of Hazardous Materials",
issn = "0304-3894",
publisher = "Elsevier",

}

Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments. / Xiang, Qian; Zhu, Dong; Giles, Madeline; Neilson, Roy; Yang, Xiao-Ru; Qiao, Min; Chen, Qing-Lin (Lead / Corresponding author).

In: Journal of Hazardous Materials, Vol. 382, 121068, 15.01.2020, p. 1-8.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments

AU - Xiang, Qian

AU - Zhu, Dong

AU - Giles, Madeline

AU - Neilson, Roy

AU - Yang, Xiao-Ru

AU - Qiao, Min

AU - Chen, Qing-Lin

N1 - This research was funded by the National Key Research and Development Program of China (2017YFE0107300), Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020402), Water Science and Technology Fund of Jiangxi Province in China (KT201702) and the Natural Environment Research Council (NE/N00745X/1 and NE/S009132). The James Hutton Institute receives financial support from the Scottish Government Rural and Environment Science and Analytical Services Division. Copyright © 2019 Elsevier B.V. All rights reserved.

PY - 2019/8/21

Y1 - 2019/8/21

N2 - The plant microbiome represents a crucial pathway for human exposure to environmental antibiotic resistance. However, little information is available regarding the plant associated resistome in human-related environments at a larger scale. Here, by high-throughput quantitative-PCR chip-based array and amplicon sequencing, we characterized antibiotic resistance genes (ARGs) and bacterial communities in plant and soil microbiomes from human highly disturbed peri-urban farmland and less disturbed forest at a watershed scale. A total of 71 ARGs were detected in the phyllosphere, which covered almost all the major recognized classes of antibiotics that are administered commonly to humans and animals. The overall pattern of the plant associated resistome in intensive anthropogenic influenced farmland was significantly different from that of forest environments (PERMANOVA, P < 0.01), indicating that agricultural activities might be important drivers in shaping the plant resistome. A bipartite network analysis suggested that all ARGs detected in the plant microbiome were also present in the soil microbiome. Together, our findings provide a better understanding of the plant resistome and suggest that land use is a key contributor to the composition of ARG profiles in the plant phyllosphere, and that the soil resistome may represent a critical reservoir of plant associated ARGs.

AB - The plant microbiome represents a crucial pathway for human exposure to environmental antibiotic resistance. However, little information is available regarding the plant associated resistome in human-related environments at a larger scale. Here, by high-throughput quantitative-PCR chip-based array and amplicon sequencing, we characterized antibiotic resistance genes (ARGs) and bacterial communities in plant and soil microbiomes from human highly disturbed peri-urban farmland and less disturbed forest at a watershed scale. A total of 71 ARGs were detected in the phyllosphere, which covered almost all the major recognized classes of antibiotics that are administered commonly to humans and animals. The overall pattern of the plant associated resistome in intensive anthropogenic influenced farmland was significantly different from that of forest environments (PERMANOVA, P < 0.01), indicating that agricultural activities might be important drivers in shaping the plant resistome. A bipartite network analysis suggested that all ARGs detected in the plant microbiome were also present in the soil microbiome. Together, our findings provide a better understanding of the plant resistome and suggest that land use is a key contributor to the composition of ARG profiles in the plant phyllosphere, and that the soil resistome may represent a critical reservoir of plant associated ARGs.

U2 - 10.1016/j.jhazmat.2019.121068

DO - 10.1016/j.jhazmat.2019.121068

M3 - Article

VL - 382

SP - 1

EP - 8

JO - Journal of Hazardous Materials

JF - Journal of Hazardous Materials

SN - 0304-3894

M1 - 121068

ER -