Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils

Yi Zhao; Tatiana Cocerva; Siobhan Cox; Stacie Tardif; Jian Qiang Su; Yong Guan Zhu; Kristian Koefoed Brandt

doi:10.1016/j.scitotenv.2018.11.372

Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils

Yi Zhao^*, Tatiana Cocerva, Siobhan Cox, Stacie Tardif, Jian Qiang Su, Yong Guan Zhu, Kristian Koefoed Brandt

^*Corresponding author for this work

54 Citations (Scopus)

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Abstract

Antibiotic resistance genes (ARGs) constitute emerging environmental pollutants and pose risks to public health. Toxic metals are known to select for metal-resistant bacteria in metal-contaminated soils, but there is growing concern that metal contaminants can also act as co-selective agents thereby causing environmental proliferation of antibiotic resistance. In this study, we quantified ARGs and selected mobile genetic elements (MGEs) known to constitute potential ARG hosts in 50 archived urban and suburban soils from the Belfast metropolitan area using a high-throughput qPCR ARG chip. ARG prevalence was linked to concentrations of individual metals and a soil metal toxicity index calculated based on the relative toxicity of different metals to soil microbial processes. A total of 164 ARGs were detected across the 50 soils analyzed with an average absolute abundance of 3.4 × 10⁷ ARG gene copies per gram of soil. A significant correlation between abundance of ARGs and MGEs was observed, suggesting the importance of horizontal gene transfer for ARG dissemination. Network analysis revealed significant co-occurrence patterns between specific metals (As, Cd, Co, Cr, Cu. Hg, Ni and Zn) and associated ARGs. Path analysis further indicated that the soil metal toxicity index significantly affected the number of detected ARGs (λ = 0.32, P < 0.001) and the abundance of metal co-occurring ARGs (λ = 0.612, P < 0.001) via effects on MGEs. Collectively, our results indicate a role of soil metals in co-selection of ARGs and MGEs in urban and semi-urban soils and suggest a risk for environmental ARG dissemination via horizontal gene transfer.

Original language	English
Journal	Science of the Total Environment
Volume	656
Pages (from-to)	512-520
ISSN	0048-9697
DOIs	https://doi.org/10.1016/j.scitotenv.2018.11.372
Publication status	Published - 15 Mar 2019

Keywords

Antibiotic resistance genes
Co-selection
Metal toxicity
Mobile genetic elements
qPCR chip
Urban soils

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.scitotenv.2018.11.372

ZhaoYetal2019_Self-ArchivingAccepted author manuscript, 1.3 MBLicence: CC BY-NC-ND

https://pureadmin.qub.ac.uk/ws/files/166432320/STOTEN_S_18_10468.pdf

Cite this

@article{6f03e1e895f949828e4ccb545681d833,

title = "Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils",

abstract = "Antibiotic resistance genes (ARGs) constitute emerging environmental pollutants and pose risks to public health. Toxic metals are known to select for metal-resistant bacteria in metal-contaminated soils, but there is growing concern that metal contaminants can also act as co-selective agents thereby causing environmental proliferation of antibiotic resistance. In this study, we quantified ARGs and selected mobile genetic elements (MGEs) known to constitute potential ARG hosts in 50 archived urban and suburban soils from the Belfast metropolitan area using a high-throughput qPCR ARG chip. ARG prevalence was linked to concentrations of individual metals and a soil metal toxicity index calculated based on the relative toxicity of different metals to soil microbial processes. A total of 164 ARGs were detected across the 50 soils analyzed with an average absolute abundance of 3.4 × 107 ARG gene copies per gram of soil. A significant correlation between abundance of ARGs and MGEs was observed, suggesting the importance of horizontal gene transfer for ARG dissemination. Network analysis revealed significant co-occurrence patterns between specific metals (As, Cd, Co, Cr, Cu. Hg, Ni and Zn) and associated ARGs. Path analysis further indicated that the soil metal toxicity index significantly affected the number of detected ARGs (λ = 0.32, P < 0.001) and the abundance of metal co-occurring ARGs (λ = 0.612, P < 0.001) via effects on MGEs. Collectively, our results indicate a role of soil metals in co-selection of ARGs and MGEs in urban and semi-urban soils and suggest a risk for environmental ARG dissemination via horizontal gene transfer.",

keywords = "Antibiotic resistance genes, Co-selection, Metal toxicity, Mobile genetic elements, qPCR chip, Urban soils",

author = "Yi Zhao and Tatiana Cocerva and Siobhan Cox and Stacie Tardif and Su, {Jian Qiang} and Zhu, {Yong Guan} and Brandt, {Kristian Koefoed}",

year = "2019",

month = mar,

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doi = "10.1016/j.scitotenv.2018.11.372",

language = "English",

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T1 - Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils

AU - Zhao, Yi

AU - Cocerva, Tatiana

AU - Cox, Siobhan

AU - Tardif, Stacie

AU - Su, Jian Qiang

AU - Zhu, Yong Guan

AU - Brandt, Kristian Koefoed

PY - 2019/3/15

Y1 - 2019/3/15

N2 - Antibiotic resistance genes (ARGs) constitute emerging environmental pollutants and pose risks to public health. Toxic metals are known to select for metal-resistant bacteria in metal-contaminated soils, but there is growing concern that metal contaminants can also act as co-selective agents thereby causing environmental proliferation of antibiotic resistance. In this study, we quantified ARGs and selected mobile genetic elements (MGEs) known to constitute potential ARG hosts in 50 archived urban and suburban soils from the Belfast metropolitan area using a high-throughput qPCR ARG chip. ARG prevalence was linked to concentrations of individual metals and a soil metal toxicity index calculated based on the relative toxicity of different metals to soil microbial processes. A total of 164 ARGs were detected across the 50 soils analyzed with an average absolute abundance of 3.4 × 107 ARG gene copies per gram of soil. A significant correlation between abundance of ARGs and MGEs was observed, suggesting the importance of horizontal gene transfer for ARG dissemination. Network analysis revealed significant co-occurrence patterns between specific metals (As, Cd, Co, Cr, Cu. Hg, Ni and Zn) and associated ARGs. Path analysis further indicated that the soil metal toxicity index significantly affected the number of detected ARGs (λ = 0.32, P < 0.001) and the abundance of metal co-occurring ARGs (λ = 0.612, P < 0.001) via effects on MGEs. Collectively, our results indicate a role of soil metals in co-selection of ARGs and MGEs in urban and semi-urban soils and suggest a risk for environmental ARG dissemination via horizontal gene transfer.

AB - Antibiotic resistance genes (ARGs) constitute emerging environmental pollutants and pose risks to public health. Toxic metals are known to select for metal-resistant bacteria in metal-contaminated soils, but there is growing concern that metal contaminants can also act as co-selective agents thereby causing environmental proliferation of antibiotic resistance. In this study, we quantified ARGs and selected mobile genetic elements (MGEs) known to constitute potential ARG hosts in 50 archived urban and suburban soils from the Belfast metropolitan area using a high-throughput qPCR ARG chip. ARG prevalence was linked to concentrations of individual metals and a soil metal toxicity index calculated based on the relative toxicity of different metals to soil microbial processes. A total of 164 ARGs were detected across the 50 soils analyzed with an average absolute abundance of 3.4 × 107 ARG gene copies per gram of soil. A significant correlation between abundance of ARGs and MGEs was observed, suggesting the importance of horizontal gene transfer for ARG dissemination. Network analysis revealed significant co-occurrence patterns between specific metals (As, Cd, Co, Cr, Cu. Hg, Ni and Zn) and associated ARGs. Path analysis further indicated that the soil metal toxicity index significantly affected the number of detected ARGs (λ = 0.32, P < 0.001) and the abundance of metal co-occurring ARGs (λ = 0.612, P < 0.001) via effects on MGEs. Collectively, our results indicate a role of soil metals in co-selection of ARGs and MGEs in urban and semi-urban soils and suggest a risk for environmental ARG dissemination via horizontal gene transfer.

KW - Antibiotic resistance genes

KW - Co-selection

KW - Metal toxicity

KW - Mobile genetic elements

KW - qPCR chip

KW - Urban soils

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DO - 10.1016/j.scitotenv.2018.11.372

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SN - 0048-9697

VL - 656

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EP - 520

JO - Science of the Total Environment

JF - Science of the Total Environment

ER -

Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils

Abstract

Keywords

UN SDGs

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