Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum

Rice paddy soil is a hotspot of antibiotic resistance genes (ARGs) due to the application of organic fertilizers. However, the temporal dynamics of ARGs in rice paddy soil and its flooded water during the growing season remain underexplored. In this study, a microcosm experiment was conducted to exp...

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Main Authors: Qian Xiang, Chen-Xi Fu, Chang-Yi Lu, An-Qi Sun, Qing-Lin Chen, Min Qiao
Format: Article
Language:English
Published: Elsevier 2023-09-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412023004415
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author Qian Xiang
Chen-Xi Fu
Chang-Yi Lu
An-Qi Sun
Qing-Lin Chen
Min Qiao
author_facet Qian Xiang
Chen-Xi Fu
Chang-Yi Lu
An-Qi Sun
Qing-Lin Chen
Min Qiao
author_sort Qian Xiang
collection DOAJ
description Rice paddy soil is a hotspot of antibiotic resistance genes (ARGs) due to the application of organic fertilizers. However, the temporal dynamics of ARGs in rice paddy soil and its flooded water during the growing season remain underexplored. In this study, a microcosm experiment was conducted to explore the ARG profiles in a long term (130 days) flooded two-phase manure-amended soil–water system. By using high-throughput quantitative PCR array, a total of 23–98 and 34–85 ARGs were detected in the soil and overlying water, respectively. Regression analysis exhibited significant negative correlations between ARG profile similarities and flooding duration, indicating that flooding significantly altered the resistome (P < 0.001). This finding was validated by the increased ARG abundance in the soil and the overlying water, for example, after 130 days flooding, the abundance of ARGs in CK soil was increased from 0.03 to 1.20 copies per 16S rRNA. The PCoA analysis further suggested pig manure application resulted in distinct ARG profiles in the soil–water continuum compared with those of the non-amended control (Adonis, P < 0.05). The Venn diagram showed that all ARGs detected in the pig manure were present in the treated soil. Twelve ARGs (e.g., sul1) were shared among the pig manure, manure-amended soil, and overlying water, indicating that certain manure- or soil-borne ARGs were readily dispersed from the soil to the overlying water. Moreover, the enhanced relationships between the ARGs and mobile genetic elements in pig manure applied soil–water continuum indicate that the application of organic matter could accelerate the emergence and dissemination of ARGs. These findings suggested that flooding represents a crucial pathway for dispersal of ARGs from the soil to the overlying water. Identification of highly mobile ARGs in the soil–water continuum is essential for assessing their potential risk to human health and promoting the development of sustainable agricultural practices to mitigate their spread.
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spelling doaj.art-c8aa05747d184cee9bff4eb9a29ea76b2023-09-16T05:28:45ZengElsevierEnvironment International0160-41202023-09-01179108168Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuumQian Xiang0Chen-Xi Fu1Chang-Yi Lu2An-Qi Sun3Qing-Lin Chen4Min Qiao5Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China; Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo 315830, ChinaState Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaKey Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China; Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo 315830, ChinaKey Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China; Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo 315830, ChinaKey Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China; Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo 315830, China; Corresponding authors at: Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China (Q. Chen). State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China (M. Qiao).State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; University of Chinese Academy of Sciences, Beijing 100049, China; Corresponding authors at: Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China (Q. Chen). State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China (M. Qiao).Rice paddy soil is a hotspot of antibiotic resistance genes (ARGs) due to the application of organic fertilizers. However, the temporal dynamics of ARGs in rice paddy soil and its flooded water during the growing season remain underexplored. In this study, a microcosm experiment was conducted to explore the ARG profiles in a long term (130 days) flooded two-phase manure-amended soil–water system. By using high-throughput quantitative PCR array, a total of 23–98 and 34–85 ARGs were detected in the soil and overlying water, respectively. Regression analysis exhibited significant negative correlations between ARG profile similarities and flooding duration, indicating that flooding significantly altered the resistome (P < 0.001). This finding was validated by the increased ARG abundance in the soil and the overlying water, for example, after 130 days flooding, the abundance of ARGs in CK soil was increased from 0.03 to 1.20 copies per 16S rRNA. The PCoA analysis further suggested pig manure application resulted in distinct ARG profiles in the soil–water continuum compared with those of the non-amended control (Adonis, P < 0.05). The Venn diagram showed that all ARGs detected in the pig manure were present in the treated soil. Twelve ARGs (e.g., sul1) were shared among the pig manure, manure-amended soil, and overlying water, indicating that certain manure- or soil-borne ARGs were readily dispersed from the soil to the overlying water. Moreover, the enhanced relationships between the ARGs and mobile genetic elements in pig manure applied soil–water continuum indicate that the application of organic matter could accelerate the emergence and dissemination of ARGs. These findings suggested that flooding represents a crucial pathway for dispersal of ARGs from the soil to the overlying water. Identification of highly mobile ARGs in the soil–water continuum is essential for assessing their potential risk to human health and promoting the development of sustainable agricultural practices to mitigate their spread.http://www.sciencedirect.com/science/article/pii/S0160412023004415Soil–water resistomeTemporal dynamicsOrganic fertilizationAntibiotic resistance gene transferBacterial community
spellingShingle Qian Xiang
Chen-Xi Fu
Chang-Yi Lu
An-Qi Sun
Qing-Lin Chen
Min Qiao
Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
Environment International
Soil–water resistome
Temporal dynamics
Organic fertilization
Antibiotic resistance gene transfer
Bacterial community
title Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
title_full Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
title_fullStr Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
title_full_unstemmed Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
title_short Flooding drives the temporal turnover of antibiotic resistance gene in manure-amended soil–water continuum
title_sort flooding drives the temporal turnover of antibiotic resistance gene in manure amended soil water continuum
topic Soil–water resistome
Temporal dynamics
Organic fertilization
Antibiotic resistance gene transfer
Bacterial community
url http://www.sciencedirect.com/science/article/pii/S0160412023004415
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