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Short-Term Benzalkonium Chloride (C12) Exposure Induced the Occurrence of Wide-Spectrum Antibiotic Resistance in Agricultural Soils
Antibiotic resistance genes (ARGs) are global pollutants that pose a potential risk to human health. Benzalkonium chloride (C12) (BC) disinfectants are thought to exert selection pressure on antibiotic resistance. However, evidence of BC-induced changes in antibiotic resistance in the soil environme...
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Published in: | Environmental science & technology 2022-11, Vol.56 (21), p.15054-15063 |
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description | Antibiotic resistance genes (ARGs) are global pollutants that pose a potential risk to human health. Benzalkonium chloride (C12) (BC) disinfectants are thought to exert selection pressure on antibiotic resistance. However, evidence of BC-induced changes in antibiotic resistance in the soil environment is lacking. Here, we established short-term soil microcosms to investigate ARG profile dynamics in agricultural soils amended with sulfamethazine (SMZ, 10 mg kg–1) and gradient concentrations of BC (0–100 mg kg–1), using high-throughput quantitative PCR and Illumina sequencing. With the increase in BC concentration, the number of ARGs detected in the soil increased, but the normalized ARG abundance decreased. The added SMZ had a limited impact on ARG profiles. Compared to broad-spectrum fungicidal BC, the specificity of SMZ significantly affected the microbial community. Network analysis found that low–medium BC exposure concentrations resulted in the formation of small but strong ARG co-occurrence clusters in the soil, while high BC exposure concentration led to a higher incidence of ARGs. Variation partitioning analysis suggested that BC stress was the major driver shaping the ARG profile. Overall, this study highlighted the emergence and spread of BC-induced ARGs, potentially leading to the antimicrobial resistance problem in agricultural soils. |
doi_str_mv | 10.1021/acs.est.2c04730 |
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Benzalkonium chloride (C12) (BC) disinfectants are thought to exert selection pressure on antibiotic resistance. However, evidence of BC-induced changes in antibiotic resistance in the soil environment is lacking. Here, we established short-term soil microcosms to investigate ARG profile dynamics in agricultural soils amended with sulfamethazine (SMZ, 10 mg kg–1) and gradient concentrations of BC (0–100 mg kg–1), using high-throughput quantitative PCR and Illumina sequencing. With the increase in BC concentration, the number of ARGs detected in the soil increased, but the normalized ARG abundance decreased. The added SMZ had a limited impact on ARG profiles. Compared to broad-spectrum fungicidal BC, the specificity of SMZ significantly affected the microbial community. Network analysis found that low–medium BC exposure concentrations resulted in the formation of small but strong ARG co-occurrence clusters in the soil, while high BC exposure concentration led to a higher incidence of ARGs. Variation partitioning analysis suggested that BC stress was the major driver shaping the ARG profile. Overall, this study highlighted the emergence and spread of BC-induced ARGs, potentially leading to the antimicrobial resistance problem in agricultural soils.</description><identifier>ISSN: 0013-936X</identifier><identifier>EISSN: 1520-5851</identifier><identifier>DOI: 10.1021/acs.est.2c04730</identifier><language>eng</language><publisher>Easton: American Chemical Society</publisher><subject>Agricultural land ; Antibiotic resistance ; Antibiotics ; Antimicrobial resistance ; Benzalkonium chloride ; Contaminants in Aquatic and Terrestrial Environments ; Disinfectants ; Drug resistance ; Exposure ; Fungicides ; Health risks ; Microcosms ; Microorganisms ; Network analysis ; Pollutants ; Sequences ; Soil amendment ; Soil contamination ; Soil dynamics ; Soil environment ; Soil investigations ; Soil pollution ; Soil resistance ; Soils ; Sulfamethazine</subject><ispartof>Environmental science & technology, 2022-11, Vol.56 (21), p.15054-15063</ispartof><rights>2022 American Chemical Society</rights><rights>Copyright American Chemical Society Nov 1, 2022</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a268t-ae05e31e16501a6ccc69b4e2a4710fbd96d04285d7fd5b71e5d31934ac55d2f13</citedby><cites>FETCH-LOGICAL-a268t-ae05e31e16501a6ccc69b4e2a4710fbd96d04285d7fd5b71e5d31934ac55d2f13</cites><orcidid>0000-0003-1875-249X ; 0000-0003-0427-4597 ; 0000-0002-1932-8765</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Zeng, Jieyi</creatorcontrib><creatorcontrib>Li, Yaying</creatorcontrib><creatorcontrib>Jin, Guoping</creatorcontrib><creatorcontrib>Su, Jian-Qiang</creatorcontrib><creatorcontrib>Yao, Huaiying</creatorcontrib><title>Short-Term Benzalkonium Chloride (C12) Exposure Induced the Occurrence of Wide-Spectrum Antibiotic Resistance in Agricultural Soils</title><title>Environmental science & technology</title><addtitle>Environ. Sci. Technol</addtitle><description>Antibiotic resistance genes (ARGs) are global pollutants that pose a potential risk to human health. Benzalkonium chloride (C12) (BC) disinfectants are thought to exert selection pressure on antibiotic resistance. However, evidence of BC-induced changes in antibiotic resistance in the soil environment is lacking. Here, we established short-term soil microcosms to investigate ARG profile dynamics in agricultural soils amended with sulfamethazine (SMZ, 10 mg kg–1) and gradient concentrations of BC (0–100 mg kg–1), using high-throughput quantitative PCR and Illumina sequencing. With the increase in BC concentration, the number of ARGs detected in the soil increased, but the normalized ARG abundance decreased. The added SMZ had a limited impact on ARG profiles. Compared to broad-spectrum fungicidal BC, the specificity of SMZ significantly affected the microbial community. Network analysis found that low–medium BC exposure concentrations resulted in the formation of small but strong ARG co-occurrence clusters in the soil, while high BC exposure concentration led to a higher incidence of ARGs. Variation partitioning analysis suggested that BC stress was the major driver shaping the ARG profile. Overall, this study highlighted the emergence and spread of BC-induced ARGs, potentially leading to the antimicrobial resistance problem in agricultural soils.</description><subject>Agricultural land</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antimicrobial resistance</subject><subject>Benzalkonium chloride</subject><subject>Contaminants in Aquatic and Terrestrial Environments</subject><subject>Disinfectants</subject><subject>Drug resistance</subject><subject>Exposure</subject><subject>Fungicides</subject><subject>Health risks</subject><subject>Microcosms</subject><subject>Microorganisms</subject><subject>Network analysis</subject><subject>Pollutants</subject><subject>Sequences</subject><subject>Soil amendment</subject><subject>Soil contamination</subject><subject>Soil dynamics</subject><subject>Soil environment</subject><subject>Soil investigations</subject><subject>Soil pollution</subject><subject>Soil resistance</subject><subject>Soils</subject><subject>Sulfamethazine</subject><issn>0013-936X</issn><issn>1520-5851</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kM9LwzAUx4MoOKdnrwEvinTLj6bdjrNMHQwGbqK3kiavLrNrZpKCevUft2XDm_DgHd7n-33wQeiSkgEljA6l8gPwYcAUiVNOjlCPCkYiMRL0GPUIoTwa8-T1FJ15vyGEME5GPfSzXFsXohW4Lb6D-ltW77Y2zRZn68o6owFfZ5Td4OnnzvrGAZ7VulGgcVgDXijVOAe1AmxL_NLS0XIHKrg2P6mDKYwNRuEn8MYH2WGmxpM3Z1RThcbJCi-tqfw5Oill5eHisPvo-X66yh6j-eJhlk3mkWTJKEQSiABOgSaCUJkopZJxEQOTcUpJWehxoknMRkKnpRZFSkFoTsc8lkoIzUrK--hq37tz9qNpXeUb27i6fZmzlNM4TdppqeGeUs5676DMd85spfvKKck703lrOu_SB9Nt4naf6A5_lf_Rv28vgnA</recordid><startdate>20221101</startdate><enddate>20221101</enddate><creator>Zeng, Jieyi</creator><creator>Li, Yaying</creator><creator>Jin, Guoping</creator><creator>Su, Jian-Qiang</creator><creator>Yao, Huaiying</creator><general>American Chemical Society</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7ST</scope><scope>7T7</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0003-1875-249X</orcidid><orcidid>https://orcid.org/0000-0003-0427-4597</orcidid><orcidid>https://orcid.org/0000-0002-1932-8765</orcidid></search><sort><creationdate>20221101</creationdate><title>Short-Term Benzalkonium Chloride (C12) Exposure Induced the Occurrence of Wide-Spectrum Antibiotic Resistance in Agricultural Soils</title><author>Zeng, Jieyi ; Li, Yaying ; Jin, Guoping ; Su, Jian-Qiang ; Yao, Huaiying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a268t-ae05e31e16501a6ccc69b4e2a4710fbd96d04285d7fd5b71e5d31934ac55d2f13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Agricultural land</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Antimicrobial resistance</topic><topic>Benzalkonium chloride</topic><topic>Contaminants in Aquatic and Terrestrial Environments</topic><topic>Disinfectants</topic><topic>Drug resistance</topic><topic>Exposure</topic><topic>Fungicides</topic><topic>Health risks</topic><topic>Microcosms</topic><topic>Microorganisms</topic><topic>Network analysis</topic><topic>Pollutants</topic><topic>Sequences</topic><topic>Soil amendment</topic><topic>Soil contamination</topic><topic>Soil dynamics</topic><topic>Soil environment</topic><topic>Soil investigations</topic><topic>Soil pollution</topic><topic>Soil resistance</topic><topic>Soils</topic><topic>Sulfamethazine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zeng, Jieyi</creatorcontrib><creatorcontrib>Li, Yaying</creatorcontrib><creatorcontrib>Jin, Guoping</creatorcontrib><creatorcontrib>Su, Jian-Qiang</creatorcontrib><creatorcontrib>Yao, Huaiying</creatorcontrib><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><jtitle>Environmental science & technology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zeng, Jieyi</au><au>Li, Yaying</au><au>Jin, Guoping</au><au>Su, Jian-Qiang</au><au>Yao, Huaiying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Short-Term Benzalkonium Chloride (C12) Exposure Induced the Occurrence of Wide-Spectrum Antibiotic Resistance in Agricultural Soils</atitle><jtitle>Environmental science & technology</jtitle><addtitle>Environ. Sci. Technol</addtitle><date>2022-11-01</date><risdate>2022</risdate><volume>56</volume><issue>21</issue><spage>15054</spage><epage>15063</epage><pages>15054-15063</pages><issn>0013-936X</issn><eissn>1520-5851</eissn><abstract>Antibiotic resistance genes (ARGs) are global pollutants that pose a potential risk to human health. Benzalkonium chloride (C12) (BC) disinfectants are thought to exert selection pressure on antibiotic resistance. However, evidence of BC-induced changes in antibiotic resistance in the soil environment is lacking. Here, we established short-term soil microcosms to investigate ARG profile dynamics in agricultural soils amended with sulfamethazine (SMZ, 10 mg kg–1) and gradient concentrations of BC (0–100 mg kg–1), using high-throughput quantitative PCR and Illumina sequencing. With the increase in BC concentration, the number of ARGs detected in the soil increased, but the normalized ARG abundance decreased. The added SMZ had a limited impact on ARG profiles. Compared to broad-spectrum fungicidal BC, the specificity of SMZ significantly affected the microbial community. Network analysis found that low–medium BC exposure concentrations resulted in the formation of small but strong ARG co-occurrence clusters in the soil, while high BC exposure concentration led to a higher incidence of ARGs. Variation partitioning analysis suggested that BC stress was the major driver shaping the ARG profile. Overall, this study highlighted the emergence and spread of BC-induced ARGs, potentially leading to the antimicrobial resistance problem in agricultural soils.</abstract><cop>Easton</cop><pub>American Chemical Society</pub><doi>10.1021/acs.est.2c04730</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-1875-249X</orcidid><orcidid>https://orcid.org/0000-0003-0427-4597</orcidid><orcidid>https://orcid.org/0000-0002-1932-8765</orcidid></addata></record> |
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subjects | Agricultural land Antibiotic resistance Antibiotics Antimicrobial resistance Benzalkonium chloride Contaminants in Aquatic and Terrestrial Environments Disinfectants Drug resistance Exposure Fungicides Health risks Microcosms Microorganisms Network analysis Pollutants Sequences Soil amendment Soil contamination Soil dynamics Soil environment Soil investigations Soil pollution Soil resistance Soils Sulfamethazine |
title | Short-Term Benzalkonium Chloride (C12) Exposure Induced the Occurrence of Wide-Spectrum Antibiotic Resistance in Agricultural Soils |
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