Insights into microbial contamination in multi-type manure-amended soils: The profile of human bacterial pathogens, virulence factor genes and antibiotic resistance genes

Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and...

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Published in	Journal of hazardous materials Vol. 437; p. 129356
Main Authors	Zhu, Lin, Lian, Yulu, Lin, Da, Huang, Dan, Yao, Yanlai, Ju, Feng, Wang, Meizhen
Format	Journal Article
Language	English
Published	Elsevier B.V 05.09.2022
Subjects	agricultural soils antibiotic resistance Antibiotic resistance genes cow manure excreta Human bacterial pathogens humans Manure microbial contamination Microbiological risk mineral fertilizers pig manure poultry manure risk silkworms vancomycin virulence Virulence factor genes Human bacterial pathogens Microbiological risk Manure Virulence factor genes Antibiotic resistance genes
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ISSN	0304-3894 1873-3336 1873-3336
DOI	10.1016/j.jhazmat.2022.129356

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Abstract	Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and human bacterial pathogens (HBPs) in different manure-amended soils remain largely unknown. Here, we conducted the systematic metagenome-based study to explore changes in resistome, VFGs and HBPs in soils treated by frequently-used manures. The results revealed that many manure-borne ARGs, VFGs, and HBPs could be spreaded into soils, and their diversity and abundance were significantly different among chemical fertilizer, pig manure, chicken manure, cow dung and silkworm excrement application. A total of 157 potential HBPs accounting about 1.33% of total bacteria were detected. The main ARGs transferred from manures to soil conferred resistance to vancomycin and macrolide-lincosamide-streptogramin. The series analysis revealed positive co-occurrence patterns of ARGs-HBPs, VFGs-HBPs and ARGs-VFGs. Microbial contamination were more serious in pig manure and silkworm excrement sample than in the other samples, implying the usage of these two manures increased the risk of HBPs and dissemination of ARGs. This study confirmed the prevalence and discrepancy of resistome, VFGs and HBPs in different manure-amended soils. [Display omitted] •A total of 157 potential human bacterial pathogens were detected, accounting about 1.33% of total bacteria screened.•Abundant and diverse virulence factor genes and antibiotic resistance genes were identified in the agricultural soils.•The coexistence of many antibiotic resistance genes and virulence factor genes was found in human bacterial pathogens.•Pig manure and silkworm excrement increased higher microbiological risks in farmland soil.
AbstractList	Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and human bacterial pathogens (HBPs) in different manure-amended soils remain largely unknown. Here, we conducted the systematic metagenome-based study to explore changes in resistome, VFGs and HBPs in soils treated by frequently-used manures. The results revealed that many manure-borne ARGs, VFGs, and HBPs could be spreaded into soils, and their diversity and abundance were significantly different among chemical fertilizer, pig manure, chicken manure, cow dung and silkworm excrement application. A total of 157 potential HBPs accounting about 1.33% of total bacteria were detected. The main ARGs transferred from manures to soil conferred resistance to vancomycin and macrolide-lincosamide-streptogramin. The series analysis revealed positive co-occurrence patterns of ARGs-HBPs, VFGs-HBPs and ARGs-VFGs. Microbial contamination were more serious in pig manure and silkworm excrement sample than in the other samples, implying the usage of these two manures increased the risk of HBPs and dissemination of ARGs. This study confirmed the prevalence and discrepancy of resistome, VFGs and HBPs in different manure-amended soils. [Display omitted] •A total of 157 potential human bacterial pathogens were detected, accounting about 1.33% of total bacteria screened.•Abundant and diverse virulence factor genes and antibiotic resistance genes were identified in the agricultural soils.•The coexistence of many antibiotic resistance genes and virulence factor genes was found in human bacterial pathogens.•Pig manure and silkworm excrement increased higher microbiological risks in farmland soil. Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and human bacterial pathogens (HBPs) in different manure-amended soils remain largely unknown. Here, we conducted the systematic metagenome-based study to explore changes in resistome, VFGs and HBPs in soils treated by frequently-used manures. The results revealed that many manure-borne ARGs, VFGs, and HBPs could be spreaded into soils, and their diversity and abundance were significantly different among chemical fertilizer, pig manure, chicken manure, cow dung and silkworm excrement application. A total of 157 potential HBPs accounting about 1.33% of total bacteria were detected. The main ARGs transferred from manures to soil conferred resistance to vancomycin and macrolide-lincosamide-streptogramin. The series analysis revealed positive co-occurrence patterns of ARGs-HBPs, VFGs-HBPs and ARGs-VFGs. Microbial contamination were more serious in pig manure and silkworm excrement sample than in the other samples, implying the usage of these two manures increased the risk of HBPs and dissemination of ARGs. This study confirmed the prevalence and discrepancy of resistome, VFGs and HBPs in different manure-amended soils. Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and human bacterial pathogens (HBPs) in different manure-amended soils remain largely unknown. Here, we conducted the systematic metagenome-based study to explore changes in resistome, VFGs and HBPs in soils treated by frequently-used manures. The results revealed that many manure-borne ARGs, VFGs, and HBPs could be spreaded into soils, and their diversity and abundance were significantly different among chemical fertilizer, pig manure, chicken manure, cow dung and silkworm excrement application. A total of 157 potential HBPs accounting about 1.33% of total bacteria were detected. The main ARGs transferred from manures to soil conferred resistance to vancomycin and macrolide-lincosamide-streptogramin. The series analysis revealed positive co-occurrence patterns of ARGs-HBPs, VFGs-HBPs and ARGs-VFGs. Microbial contamination were more serious in pig manure and silkworm excrement sample than in the other samples, implying the usage of these two manures increased the risk of HBPs and dissemination of ARGs. This study confirmed the prevalence and discrepancy of resistome, VFGs and HBPs in different manure-amended soils.Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic resistance genes (ARGs) in agricultural soil. Nevertheless, the profile of microbial contamination including ARGs, virulence factor genes (VFGs) and human bacterial pathogens (HBPs) in different manure-amended soils remain largely unknown. Here, we conducted the systematic metagenome-based study to explore changes in resistome, VFGs and HBPs in soils treated by frequently-used manures. The results revealed that many manure-borne ARGs, VFGs, and HBPs could be spreaded into soils, and their diversity and abundance were significantly different among chemical fertilizer, pig manure, chicken manure, cow dung and silkworm excrement application. A total of 157 potential HBPs accounting about 1.33% of total bacteria were detected. The main ARGs transferred from manures to soil conferred resistance to vancomycin and macrolide-lincosamide-streptogramin. The series analysis revealed positive co-occurrence patterns of ARGs-HBPs, VFGs-HBPs and ARGs-VFGs. Microbial contamination were more serious in pig manure and silkworm excrement sample than in the other samples, implying the usage of these two manures increased the risk of HBPs and dissemination of ARGs. This study confirmed the prevalence and discrepancy of resistome, VFGs and HBPs in different manure-amended soils.
ArticleNumber	129356
Author	Zhu, Lin Lian, Yulu Lin, Da Wang, Meizhen Huang, Dan Yao, Yanlai Ju, Feng
Author_xml	– sequence: 1 givenname: Lin surname: Zhu fullname: Zhu, Lin organization: School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China – sequence: 2 givenname: Yulu surname: Lian fullname: Lian, Yulu organization: School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China – sequence: 3 givenname: Da surname: Lin fullname: Lin, Da organization: School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China – sequence: 4 givenname: Dan surname: Huang fullname: Huang, Dan organization: School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China – sequence: 5 givenname: Yanlai surname: Yao fullname: Yao, Yanlai organization: Institute of Environment, Resource, Soil and Fertilizer, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China – sequence: 6 givenname: Feng surname: Ju fullname: Ju, Feng organization: Key laboratory of Coastal Environment and Resources of Zhejiang Province, School of Engineering, Westlake University, Hangzhou 310024, China – sequence: 7 givenname: Meizhen surname: Wang fullname: Wang, Meizhen email: wmz@mail.zjgsu.edu.cn organization: School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China
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Snippet	Concerns regarding biological risk in environment have garnered increasing attention. Manure has been believed to be a significant source of antibiotic...
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StartPage	129356
SubjectTerms	agricultural soils antibiotic resistance Antibiotic resistance genes cow manure excreta Human bacterial pathogens humans Manure microbial contamination Microbiological risk mineral fertilizers pig manure poultry manure risk silkworms vancomycin virulence Virulence factor genes
Title	Insights into microbial contamination in multi-type manure-amended soils: The profile of human bacterial pathogens, virulence factor genes and antibiotic resistance genes
URI	https://dx.doi.org/10.1016/j.jhazmat.2022.129356 https://www.proquest.com/docview/2679703037 https://www.proquest.com/docview/2718242509
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