Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine
The effects of pharmaceuticals as emerging contaminants in soil on the gut microbiome and antibiotic resistome in nontarget soil fauna are largely elusive. In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the m...
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| Veröffentlicht in: | Environmental science & technology 2020-09, Vol.54 (17), p.10754-10762 |
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| creator | Wang, Yi-Fei Qiao, Min Zhu, Dong Zhu, Yong-Guan |
| description | The effects of pharmaceuticals as emerging contaminants in soil on the gut microbiome and antibiotic resistome in nontarget soil fauna are largely elusive. In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the model soil collembolan (Folsomia candida) upon antiepileptic drug carbamazepine (CBZ) and antibiotic tetracycline (TC) exposure. Results showed that, individually or in combination, exposure to TC or CBZ significantly altered the gut community structure of F. candida, causing some enrichment of the bacteria associated with xenobiotic metabolism, such as Arthrobacter, Achromobacter, Gordonia, and Shinella. More importantly, oral exposure to the nonantibiotic drug CBZ enhanced the abundance and diversity of ARGs in the gut of F. candida, especially for the beta-lactams and multidrug resistance genes. Our results revealed that the most likely hosts of ARGs in the gut of F. candida were Proteobacteria and Actinobacteria. The significant positive correlation between mobile genetic elements (MGEs) and ARGs indicated the potential risk of ARGs transmission in the gut of F. candida. Overall, the nonantibiotic CBZ is likely to disturb the gut microbiota of nontarget soil fauna such as collembolans, thereby enhancing the dissemination of ARGs. |
| doi_str_mv | 10.1021/acs.est.0c03075 |
| format | Article |
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In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the model soil collembolan (Folsomia candida) upon antiepileptic drug carbamazepine (CBZ) and antibiotic tetracycline (TC) exposure. Results showed that, individually or in combination, exposure to TC or CBZ significantly altered the gut community structure of F. candida, causing some enrichment of the bacteria associated with xenobiotic metabolism, such as Arthrobacter, Achromobacter, Gordonia, and Shinella. More importantly, oral exposure to the nonantibiotic drug CBZ enhanced the abundance and diversity of ARGs in the gut of F. candida, especially for the beta-lactams and multidrug resistance genes. Our results revealed that the most likely hosts of ARGs in the gut of F. candida were Proteobacteria and Actinobacteria. The significant positive correlation between mobile genetic elements (MGEs) and ARGs indicated the potential risk of ARGs transmission in the gut of F. candida. Overall, the nonantibiotic CBZ is likely to disturb the gut microbiota of nontarget soil fauna such as collembolans, thereby enhancing the dissemination of ARGs.</description><identifier>ISSN: 0013-936X</identifier><identifier>EISSN: 1520-5851</identifier><identifier>DOI: 10.1021/acs.est.0c03075</identifier><identifier>PMID: 32816468</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Achromobacter ; Animals ; Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Antiepileptic agents ; Arthrobacter ; Carbamazepine ; Community structure ; Contaminants ; Drug resistance ; Drug Resistance, Microbial ; Ecotoxicology and Public Health ; Exposure ; Gastrointestinal Microbiome ; Genes ; Genes, Bacterial ; Intestinal microflora ; Metabolism ; Microbiomes ; Microbiota ; Multidrug resistance ; Pharmaceutical Preparations ; Sediment pollution ; Soil ; Soil contamination ; Soil fauna ; Soil pollution ; Soils ; β-Lactam antibiotics</subject><ispartof>Environmental science & technology, 2020-09, Vol.54 (17), p.10754-10762</ispartof><rights>Copyright American Chemical Society Sep 1, 2020</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a361t-929b10b90538e1c8e07d99e82de8891a2ec7fe1db9809f05f7daabe7104f6eed3</citedby><cites>FETCH-LOGICAL-a361t-929b10b90538e1c8e07d99e82de8891a2ec7fe1db9809f05f7daabe7104f6eed3</cites><orcidid>0000-0003-3861-8482 ; 0000-0002-4176-4248</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.est.0c03075$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.est.0c03075$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32816468$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Yi-Fei</creatorcontrib><creatorcontrib>Qiao, Min</creatorcontrib><creatorcontrib>Zhu, Dong</creatorcontrib><creatorcontrib>Zhu, Yong-Guan</creatorcontrib><title>Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine</title><title>Environmental science & technology</title><addtitle>Environ. Sci. Technol</addtitle><description>The effects of pharmaceuticals as emerging contaminants in soil on the gut microbiome and antibiotic resistome in nontarget soil fauna are largely elusive. In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the model soil collembolan (Folsomia candida) upon antiepileptic drug carbamazepine (CBZ) and antibiotic tetracycline (TC) exposure. Results showed that, individually or in combination, exposure to TC or CBZ significantly altered the gut community structure of F. candida, causing some enrichment of the bacteria associated with xenobiotic metabolism, such as Arthrobacter, Achromobacter, Gordonia, and Shinella. More importantly, oral exposure to the nonantibiotic drug CBZ enhanced the abundance and diversity of ARGs in the gut of F. candida, especially for the beta-lactams and multidrug resistance genes. Our results revealed that the most likely hosts of ARGs in the gut of F. candida were Proteobacteria and Actinobacteria. The significant positive correlation between mobile genetic elements (MGEs) and ARGs indicated the potential risk of ARGs transmission in the gut of F. candida. Overall, the nonantibiotic CBZ is likely to disturb the gut microbiota of nontarget soil fauna such as collembolans, thereby enhancing the dissemination of ARGs.</description><subject>Achromobacter</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antiepileptic agents</subject><subject>Arthrobacter</subject><subject>Carbamazepine</subject><subject>Community structure</subject><subject>Contaminants</subject><subject>Drug resistance</subject><subject>Drug Resistance, Microbial</subject><subject>Ecotoxicology and Public Health</subject><subject>Exposure</subject><subject>Gastrointestinal Microbiome</subject><subject>Genes</subject><subject>Genes, Bacterial</subject><subject>Intestinal microflora</subject><subject>Metabolism</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Multidrug resistance</subject><subject>Pharmaceutical Preparations</subject><subject>Sediment pollution</subject><subject>Soil</subject><subject>Soil contamination</subject><subject>Soil fauna</subject><subject>Soil pollution</subject><subject>Soils</subject><subject>β-Lactam antibiotics</subject><issn>0013-936X</issn><issn>1520-5851</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kDtPwzAUhS0EoqUwsyFLjCjttZ2HPVYFChIPCYHEFtnODaTkUexkKL-elJYyMd3lO-fofoScMhgz4GyirR-jb8dgQUAS7ZEhizgEkYzYPhkCMBEoEb8OyJH3CwDgAuQhGQguWRzGckg-pnVbmKJpC0uf0Be-1bVFWtS0fUc6a8oSK9OUuqbzrqX3hXVNT1dIp9ZiiU63mFGz-qEfmlr_tV267o3OtDO60l-4LGo8Jge5Lj2ebO-IvFxfPc9ugrvH-e1sehdoEbM2UFwZBkZBJCQyKxGSTCmUPEMpFdMcbZIjy4ySoHKI8iTT2mDCIMxjxEyMyPmmd-maz67Xky6aztX9ZMrDMFGhjEPWU5MN1b_kvcM8Xbqi0m6VMkjXctNebrpOb-X2ibNtb2cqzHb8r80euNgA6-Ru87-6b6ENhmw</recordid><startdate>20200901</startdate><enddate>20200901</enddate><creator>Wang, Yi-Fei</creator><creator>Qiao, Min</creator><creator>Zhu, Dong</creator><creator>Zhu, Yong-Guan</creator><general>American Chemical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><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/0000-0003-3861-8482</orcidid><orcidid>https://orcid.org/0000-0002-4176-4248</orcidid></search><sort><creationdate>20200901</creationdate><title>Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine</title><author>Wang, Yi-Fei ; Qiao, Min ; Zhu, Dong ; Zhu, Yong-Guan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a361t-929b10b90538e1c8e07d99e82de8891a2ec7fe1db9809f05f7daabe7104f6eed3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Achromobacter</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Antiepileptic agents</topic><topic>Arthrobacter</topic><topic>Carbamazepine</topic><topic>Community structure</topic><topic>Contaminants</topic><topic>Drug resistance</topic><topic>Drug Resistance, Microbial</topic><topic>Ecotoxicology and Public Health</topic><topic>Exposure</topic><topic>Gastrointestinal Microbiome</topic><topic>Genes</topic><topic>Genes, Bacterial</topic><topic>Intestinal microflora</topic><topic>Metabolism</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Multidrug resistance</topic><topic>Pharmaceutical Preparations</topic><topic>Sediment pollution</topic><topic>Soil</topic><topic>Soil contamination</topic><topic>Soil fauna</topic><topic>Soil pollution</topic><topic>Soils</topic><topic>β-Lactam antibiotics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Yi-Fei</creatorcontrib><creatorcontrib>Qiao, Min</creatorcontrib><creatorcontrib>Zhu, Dong</creatorcontrib><creatorcontrib>Zhu, Yong-Guan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><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>Wang, Yi-Fei</au><au>Qiao, Min</au><au>Zhu, Dong</au><au>Zhu, Yong-Guan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine</atitle><jtitle>Environmental science & technology</jtitle><addtitle>Environ. Sci. Technol</addtitle><date>2020-09-01</date><risdate>2020</risdate><volume>54</volume><issue>17</issue><spage>10754</spage><epage>10762</epage><pages>10754-10762</pages><issn>0013-936X</issn><eissn>1520-5851</eissn><abstract>The effects of pharmaceuticals as emerging contaminants in soil on the gut microbiome and antibiotic resistome in nontarget soil fauna are largely elusive. In this study, we explored the composition of the bacterial community and the presence of antibiotic resistance genes (ARGs) in the gut of the model soil collembolan (Folsomia candida) upon antiepileptic drug carbamazepine (CBZ) and antibiotic tetracycline (TC) exposure. Results showed that, individually or in combination, exposure to TC or CBZ significantly altered the gut community structure of F. candida, causing some enrichment of the bacteria associated with xenobiotic metabolism, such as Arthrobacter, Achromobacter, Gordonia, and Shinella. More importantly, oral exposure to the nonantibiotic drug CBZ enhanced the abundance and diversity of ARGs in the gut of F. candida, especially for the beta-lactams and multidrug resistance genes. Our results revealed that the most likely hosts of ARGs in the gut of F. candida were Proteobacteria and Actinobacteria. The significant positive correlation between mobile genetic elements (MGEs) and ARGs indicated the potential risk of ARGs transmission in the gut of F. candida. Overall, the nonantibiotic CBZ is likely to disturb the gut microbiota of nontarget soil fauna such as collembolans, thereby enhancing the dissemination of ARGs.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>32816468</pmid><doi>10.1021/acs.est.0c03075</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0003-3861-8482</orcidid><orcidid>https://orcid.org/0000-0002-4176-4248</orcidid></addata></record> |
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| subjects | Achromobacter Animals Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Antiepileptic agents Arthrobacter Carbamazepine Community structure Contaminants Drug resistance Drug Resistance, Microbial Ecotoxicology and Public Health Exposure Gastrointestinal Microbiome Genes Genes, Bacterial Intestinal microflora Metabolism Microbiomes Microbiota Multidrug resistance Pharmaceutical Preparations Sediment pollution Soil Soil contamination Soil fauna Soil pollution Soils β-Lactam antibiotics |
| title | Antibiotic Resistance in the Collembolan Gut Microbiome Accelerated by the Nonantibiotic Drug Carbamazepine |
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