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Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost

BACKGROUND: Antibiotics and antibiotic resistance genes (ARGs) used in intensive animal farming threaten human health worldwide; however, the common resistome, ARG mobility, and ARG host composition in different animal manures and mixed manure composts remain unclear. In the present study, metagenom...

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Autores principales: Qiu, Tianlei, Huo, Linhe, Guo, Yajie, Gao, Min, Wang, Guoliang, Hu, Dong, Li, Cheng, Wang, Zhanwu, Liu, Guiming, Wang, Xuming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9367140/
https://www.ncbi.nlm.nih.gov/pubmed/35953830
http://dx.doi.org/10.1186/s40793-022-00437-x
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author Qiu, Tianlei
Huo, Linhe
Guo, Yajie
Gao, Min
Wang, Guoliang
Hu, Dong
Li, Cheng
Wang, Zhanwu
Liu, Guiming
Wang, Xuming
author_facet Qiu, Tianlei
Huo, Linhe
Guo, Yajie
Gao, Min
Wang, Guoliang
Hu, Dong
Li, Cheng
Wang, Zhanwu
Liu, Guiming
Wang, Xuming
author_sort Qiu, Tianlei
collection PubMed
description BACKGROUND: Antibiotics and antibiotic resistance genes (ARGs) used in intensive animal farming threaten human health worldwide; however, the common resistome, ARG mobility, and ARG host composition in different animal manures and mixed manure composts remain unclear. In the present study, metagenomic assembly and cross-sample mapping were used to comprehensively decipher the common resistome and its potential mobility and hosts in animal manure and composts. RESULTS: In total, 201 ARGs were shared among different animal (layer, broiler, swine, beef cow, and dairy cow) manures and accounted for 86–99% of total relative abundance of ARGs. Except for multidrug, sulfonamide, and trimethoprim resistance genes, the relative abundance of most ARGs in composts was significantly lower than that in animal manure. Procrustes analysis indicated that antibiotic residues positively correlated with ARG composition in manure but not in composts. More than 75% ARG subtypes were shared between plasmids and chromosomes in our samples. Transposases could play a pivotal role in mediating the transfer of ARGs between different phyla in animal manure and composting. Cross-sample mapping to contigs carrying ARGs showed that the hosts of common resistome in manure had preference on animal species, and the dominant genus of ARG host shifted from Enterococcus in manure to Pseudomonas in composts. The broad host range and linking with diverse mobile genetic elements (MGEs) were two key factors for ARGs, such as sul1 and aadA, which could survive during composting. The multidrug resistance genes represented the dominant ARGs in pathogenic antibiotic-resistant bacteria in manure but could be effectively controlled by composting. CONCLUSIONS: Our experiments revealed the common resistome in animal manure, classified and relative quantified the ARG hosts, and assessed the mobility of ARGs. Composting can mitigate ARGs in animal manure by altering the bacterial hosts; however, persistent ARGs can escape from the removal because of diverse host range and MGEs. Our findings provide an overall background for source tracking, risk assessment, and control of livestock ARGs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00437-x.
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spelling pubmed-93671402022-08-12 Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost Qiu, Tianlei Huo, Linhe Guo, Yajie Gao, Min Wang, Guoliang Hu, Dong Li, Cheng Wang, Zhanwu Liu, Guiming Wang, Xuming Environ Microbiome Research BACKGROUND: Antibiotics and antibiotic resistance genes (ARGs) used in intensive animal farming threaten human health worldwide; however, the common resistome, ARG mobility, and ARG host composition in different animal manures and mixed manure composts remain unclear. In the present study, metagenomic assembly and cross-sample mapping were used to comprehensively decipher the common resistome and its potential mobility and hosts in animal manure and composts. RESULTS: In total, 201 ARGs were shared among different animal (layer, broiler, swine, beef cow, and dairy cow) manures and accounted for 86–99% of total relative abundance of ARGs. Except for multidrug, sulfonamide, and trimethoprim resistance genes, the relative abundance of most ARGs in composts was significantly lower than that in animal manure. Procrustes analysis indicated that antibiotic residues positively correlated with ARG composition in manure but not in composts. More than 75% ARG subtypes were shared between plasmids and chromosomes in our samples. Transposases could play a pivotal role in mediating the transfer of ARGs between different phyla in animal manure and composting. Cross-sample mapping to contigs carrying ARGs showed that the hosts of common resistome in manure had preference on animal species, and the dominant genus of ARG host shifted from Enterococcus in manure to Pseudomonas in composts. The broad host range and linking with diverse mobile genetic elements (MGEs) were two key factors for ARGs, such as sul1 and aadA, which could survive during composting. The multidrug resistance genes represented the dominant ARGs in pathogenic antibiotic-resistant bacteria in manure but could be effectively controlled by composting. CONCLUSIONS: Our experiments revealed the common resistome in animal manure, classified and relative quantified the ARG hosts, and assessed the mobility of ARGs. Composting can mitigate ARGs in animal manure by altering the bacterial hosts; however, persistent ARGs can escape from the removal because of diverse host range and MGEs. Our findings provide an overall background for source tracking, risk assessment, and control of livestock ARGs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00437-x. BioMed Central 2022-08-11 /pmc/articles/PMC9367140/ /pubmed/35953830 http://dx.doi.org/10.1186/s40793-022-00437-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/ Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Qiu, Tianlei
Huo, Linhe
Guo, Yajie
Gao, Min
Wang, Guoliang
Hu, Dong
Li, Cheng
Wang, Zhanwu
Liu, Guiming
Wang, Xuming
Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title_full Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title_fullStr Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title_full_unstemmed Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title_short Metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
title_sort metagenomic assembly reveals hosts and mobility of common antibiotic resistome in animal manure and commercial compost
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9367140/
https://www.ncbi.nlm.nih.gov/pubmed/35953830
http://dx.doi.org/10.1186/s40793-022-00437-x
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