Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure

Manure, which contains large amounts of antibiotics and antibiotic resistance genes (ARGs), is widely used in agricultural soils and may lead to the evolution and dispersal of ARGs in the soil environment. In the present study, soils that received manure or chemical fertilizers for 15 years were sam...

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Main Authors: Fenghua Wang, Wanxue Han, Shuaimin Chen, Wenxu Dong, Min Qiao, Chunsheng Hu, Binbin Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00062/full
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spelling doaj-b6cba8aad8704b0f82c486ec3dad2f902020-11-25T00:29:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-02-011110.3389/fmicb.2020.00062486880Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community StructureFenghua Wang0Wanxue Han1Wanxue Han2Shuaimin Chen3Wenxu Dong4Min Qiao5Chunsheng Hu6Binbin Liu7Key Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, ChinaKey Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaInstitute of Agricultural Resource and Environment, Jilin Academy of Agricultural Sciences, Changchun, ChinaKey Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, ChinaState Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, ChinaKey Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, ChinaManure, which contains large amounts of antibiotics and antibiotic resistance genes (ARGs), is widely used in agricultural soils and may lead to the evolution and dispersal of ARGs in the soil environment. In the present study, soils that received manure or chemical fertilizers for 15 years were sampled on the North China Plain (NCP), which is one of the primary areas of intensive agriculture in China. High-throughput quantitative PCR and sequencing technologies were employed to assess the effects of long-term manure or chemical fertilizer application on the distribution of ARGs and microbial communities. A total of 114 unique ARGs were successfully amplified from all soil samples. Manure application markedly increased the relative abundance and detectable numbers of ARGs, with up to 0.23 copies/16S rRNA gene and 81 unique ARGs. The increased abundance of ARGs in manure-fertilized soil was mainly due to the manure increasing the abundance of indigenous soil ARGs. In contrast, chemical fertilizers only moderately affected the diversity of ARGs and had no significant effect on the relative abundance of the total ARGs. In addition, manure application increased the abundance of mobile genetic elements (MGEs), which were significantly and positively correlated with most types of ARGs, indicating that horizontal gene transfer via MGEs may play an important role in the spread of ARGs. Furthermore, the application of manure and chemical fertilizers significantly affected microbial community structure, and variation partitioning analysis showed that microbial community shifts represented the major driver shaping the antibiotic resistome. Taken together, our results provide insight into the long-term effects of manure and chemical fertilization on the dissemination of ARGs in intensive agricultural ecosystems.https://www.frontiersin.org/article/10.3389/fmicb.2020.00062/fullantibiotic resistance genesmobile genetic elementsmanurechemical fertilizermicrobial community structure
collection DOAJ
language English
format Article
sources DOAJ
author Fenghua Wang
Wanxue Han
Wanxue Han
Shuaimin Chen
Wenxu Dong
Min Qiao
Chunsheng Hu
Binbin Liu
spellingShingle Fenghua Wang
Wanxue Han
Wanxue Han
Shuaimin Chen
Wenxu Dong
Min Qiao
Chunsheng Hu
Binbin Liu
Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
Frontiers in Microbiology
antibiotic resistance genes
mobile genetic elements
manure
chemical fertilizer
microbial community structure
author_facet Fenghua Wang
Wanxue Han
Wanxue Han
Shuaimin Chen
Wenxu Dong
Min Qiao
Chunsheng Hu
Binbin Liu
author_sort Fenghua Wang
title Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
title_short Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
title_full Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
title_fullStr Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
title_full_unstemmed Fifteen-Year Application of Manure and Chemical Fertilizers Differently Impacts Soil ARGs and Microbial Community Structure
title_sort fifteen-year application of manure and chemical fertilizers differently impacts soil args and microbial community structure
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-02-01
description Manure, which contains large amounts of antibiotics and antibiotic resistance genes (ARGs), is widely used in agricultural soils and may lead to the evolution and dispersal of ARGs in the soil environment. In the present study, soils that received manure or chemical fertilizers for 15 years were sampled on the North China Plain (NCP), which is one of the primary areas of intensive agriculture in China. High-throughput quantitative PCR and sequencing technologies were employed to assess the effects of long-term manure or chemical fertilizer application on the distribution of ARGs and microbial communities. A total of 114 unique ARGs were successfully amplified from all soil samples. Manure application markedly increased the relative abundance and detectable numbers of ARGs, with up to 0.23 copies/16S rRNA gene and 81 unique ARGs. The increased abundance of ARGs in manure-fertilized soil was mainly due to the manure increasing the abundance of indigenous soil ARGs. In contrast, chemical fertilizers only moderately affected the diversity of ARGs and had no significant effect on the relative abundance of the total ARGs. In addition, manure application increased the abundance of mobile genetic elements (MGEs), which were significantly and positively correlated with most types of ARGs, indicating that horizontal gene transfer via MGEs may play an important role in the spread of ARGs. Furthermore, the application of manure and chemical fertilizers significantly affected microbial community structure, and variation partitioning analysis showed that microbial community shifts represented the major driver shaping the antibiotic resistome. Taken together, our results provide insight into the long-term effects of manure and chemical fertilization on the dissemination of ARGs in intensive agricultural ecosystems.
topic antibiotic resistance genes
mobile genetic elements
manure
chemical fertilizer
microbial community structure
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00062/full
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