Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli
Summary Bacteria in nature often encounter non‐antibiotic antibacterials (NAAs), such as disinfectants and heavy metals, and they can evolve resistance via mechanisms that are also involved in antibiotic resistance. Understanding whether susceptibility to different types of antibacterials is non‐ran...
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Veröffentlicht in: | Environmental microbiology 2020-07, Vol.22 (7), p.2664-2679 |
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creator | Bischofberger, Anna M. Baumgartner, Michael Pfrunder‐Cardozo, Katia R. Allen, Richard C. Hall, Alex R. |
description | Summary
Bacteria in nature often encounter non‐antibiotic antibacterials (NAAs), such as disinfectants and heavy metals, and they can evolve resistance via mechanisms that are also involved in antibiotic resistance. Understanding whether susceptibility to different types of antibacterials is non‐randomly associated across natural and clinical bacteria is therefore important for predicting the spread of resistance, yet there is no consensus about the extent of such associations or underlying mechanisms. We tested for associations between susceptibility phenotypes of 93 natural and clinical Escherichia coli isolates to various NAAs and antibiotics. Across all compound combinations, we detected a small number of non‐random associations, including a trio of positive associations among chloramphenicol, triclosan and benzalkonium chloride. We investigated genetic mechanisms that can explain such associations using genomic information, genetic knockouts and experimental evolution. This revealed some mutations that are selected for by experimental exposure to one compound and confer cross‐resistance to other compounds. Surprisingly, these interactions were asymmetric: selection for chloramphenicol resistance conferred cross‐resistance to triclosan and benzalkonium chloride, but selection for triclosan resistance did not confer cross‐resistance to other compounds. These results identify genetic changes involved in variable cross‐resistance across antibiotics and NAAs, potentially contributing to associations in natural and clinical bacteria. |
doi_str_mv | 10.1111/1462-2920.14986 |
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Bacteria in nature often encounter non‐antibiotic antibacterials (NAAs), such as disinfectants and heavy metals, and they can evolve resistance via mechanisms that are also involved in antibiotic resistance. Understanding whether susceptibility to different types of antibacterials is non‐randomly associated across natural and clinical bacteria is therefore important for predicting the spread of resistance, yet there is no consensus about the extent of such associations or underlying mechanisms. We tested for associations between susceptibility phenotypes of 93 natural and clinical Escherichia coli isolates to various NAAs and antibiotics. Across all compound combinations, we detected a small number of non‐random associations, including a trio of positive associations among chloramphenicol, triclosan and benzalkonium chloride. We investigated genetic mechanisms that can explain such associations using genomic information, genetic knockouts and experimental evolution. This revealed some mutations that are selected for by experimental exposure to one compound and confer cross‐resistance to other compounds. Surprisingly, these interactions were asymmetric: selection for chloramphenicol resistance conferred cross‐resistance to triclosan and benzalkonium chloride, but selection for triclosan resistance did not confer cross‐resistance to other compounds. These results identify genetic changes involved in variable cross‐resistance across antibiotics and NAAs, potentially contributing to associations in natural and clinical bacteria.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14986</identifier><identifier>PMID: 32162766</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Antiseptics ; Bacteria ; Benzalkonium chloride ; Benzalkonium Compounds - pharmacology ; Chloramphenicol ; Chloramphenicol - pharmacology ; Chloromycetin ; Coliforms ; Disease resistance ; Disinfectants ; Disinfectants - pharmacology ; Drug resistance ; Drug Resistance, Bacterial - genetics ; E coli ; Escherichia coli ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Escherichia coli - isolation & purification ; Escherichia coli Infections - drug therapy ; Heavy metals ; Humans ; Metals ; Metals, Heavy - pharmacology ; Microbial Sensitivity Tests ; Mutation ; Phenotypes ; Triclosan ; Triclosan - pharmacology</subject><ispartof>Environmental microbiology, 2020-07, Vol.22 (7), p.2664-2679</ispartof><rights>2020 The Authors. published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4676-56278c49f8f0f749e618d13b49397aa75fb813375086c85e2634a3ecb1a28d1e3</citedby><cites>FETCH-LOGICAL-c4676-56278c49f8f0f749e618d13b49397aa75fb813375086c85e2634a3ecb1a28d1e3</cites><orcidid>0000-0002-4158-460X ; 0000-0002-3654-1373 ; 0000-0001-6012-7888 ; 0000-0001-5909-488X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.14986$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.14986$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32162766$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bischofberger, Anna M.</creatorcontrib><creatorcontrib>Baumgartner, Michael</creatorcontrib><creatorcontrib>Pfrunder‐Cardozo, Katia R.</creatorcontrib><creatorcontrib>Allen, Richard C.</creatorcontrib><creatorcontrib>Hall, Alex R.</creatorcontrib><title>Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Bacteria in nature often encounter non‐antibiotic antibacterials (NAAs), such as disinfectants and heavy metals, and they can evolve resistance via mechanisms that are also involved in antibiotic resistance. Understanding whether susceptibility to different types of antibacterials is non‐randomly associated across natural and clinical bacteria is therefore important for predicting the spread of resistance, yet there is no consensus about the extent of such associations or underlying mechanisms. We tested for associations between susceptibility phenotypes of 93 natural and clinical Escherichia coli isolates to various NAAs and antibiotics. Across all compound combinations, we detected a small number of non‐random associations, including a trio of positive associations among chloramphenicol, triclosan and benzalkonium chloride. We investigated genetic mechanisms that can explain such associations using genomic information, genetic knockouts and experimental evolution. This revealed some mutations that are selected for by experimental exposure to one compound and confer cross‐resistance to other compounds. Surprisingly, these interactions were asymmetric: selection for chloramphenicol resistance conferred cross‐resistance to triclosan and benzalkonium chloride, but selection for triclosan resistance did not confer cross‐resistance to other compounds. These results identify genetic changes involved in variable cross‐resistance across antibiotics and NAAs, potentially contributing to associations in natural and clinical bacteria.</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antiseptics</subject><subject>Bacteria</subject><subject>Benzalkonium chloride</subject><subject>Benzalkonium Compounds - pharmacology</subject><subject>Chloramphenicol</subject><subject>Chloramphenicol - pharmacology</subject><subject>Chloromycetin</subject><subject>Coliforms</subject><subject>Disease resistance</subject><subject>Disinfectants</subject><subject>Disinfectants - pharmacology</subject><subject>Drug resistance</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - isolation & purification</subject><subject>Escherichia coli Infections - drug therapy</subject><subject>Heavy metals</subject><subject>Humans</subject><subject>Metals</subject><subject>Metals, Heavy - pharmacology</subject><subject>Microbial Sensitivity Tests</subject><subject>Mutation</subject><subject>Phenotypes</subject><subject>Triclosan</subject><subject>Triclosan - pharmacology</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqFkU1PGzEQhq2qqHy0596QpV5JWX-s7b0gIZRSJCou7dnyOrPNoI0NthO0_4KfXIfQiJ7qy9gzj995pZeQz6z5yuo5Z1LxGe94fcrOqHfkaN95v78zfkiOc75vGqaFbj6QQ8GZ4lqpI_J8mXP06ArGkGkP5Qkg0AwhY8ENlomWSF0o2GMs6PMZXWDGMIAvtZvraEGX4DYTXUFxY6YYaHBlndx4Rv2IAb0bX6jR9TG5EtNEMcfRFcg0DnSe_RIS-iU66uOIH8nBUHXg02s9Ib--zX9efZ_d3l3fXF3ezrxUWs3a6t942Q1maAYtO1DMLJjoZSc67Zxuh94wIXTbGOVNC1wJ6QT4njleQRAn5GKn-7DuV7DwEEr1bB8SrlyabHRo_50EXNrfcWO1MLKRsgp8eRVI8XENudj7uE6herZcct5JbdquUuc7yqeYc4Jhv4E1dhuh3YZkt4HZlwjrj9O3xvb838wq0O6AJxxh-p-enf-42Qn_AR-mqYk</recordid><startdate>202007</startdate><enddate>202007</enddate><creator>Bischofberger, Anna M.</creator><creator>Baumgartner, Michael</creator><creator>Pfrunder‐Cardozo, Katia R.</creator><creator>Allen, Richard C.</creator><creator>Hall, Alex R.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4158-460X</orcidid><orcidid>https://orcid.org/0000-0002-3654-1373</orcidid><orcidid>https://orcid.org/0000-0001-6012-7888</orcidid><orcidid>https://orcid.org/0000-0001-5909-488X</orcidid></search><sort><creationdate>202007</creationdate><title>Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli</title><author>Bischofberger, Anna M. ; Baumgartner, Michael ; Pfrunder‐Cardozo, Katia R. ; Allen, Richard C. ; Hall, Alex R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4676-56278c49f8f0f749e618d13b49397aa75fb813375086c85e2634a3ecb1a28d1e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Antiseptics</topic><topic>Bacteria</topic><topic>Benzalkonium chloride</topic><topic>Benzalkonium Compounds - pharmacology</topic><topic>Chloramphenicol</topic><topic>Chloramphenicol - pharmacology</topic><topic>Chloromycetin</topic><topic>Coliforms</topic><topic>Disease resistance</topic><topic>Disinfectants</topic><topic>Disinfectants - pharmacology</topic><topic>Drug resistance</topic><topic>Drug Resistance, Bacterial - genetics</topic><topic>E coli</topic><topic>Escherichia coli</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - isolation & purification</topic><topic>Escherichia coli Infections - drug therapy</topic><topic>Heavy metals</topic><topic>Humans</topic><topic>Metals</topic><topic>Metals, Heavy - pharmacology</topic><topic>Microbial Sensitivity Tests</topic><topic>Mutation</topic><topic>Phenotypes</topic><topic>Triclosan</topic><topic>Triclosan - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bischofberger, Anna M.</creatorcontrib><creatorcontrib>Baumgartner, Michael</creatorcontrib><creatorcontrib>Pfrunder‐Cardozo, Katia R.</creatorcontrib><creatorcontrib>Allen, Richard C.</creatorcontrib><creatorcontrib>Hall, Alex R.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bischofberger, Anna M.</au><au>Baumgartner, Michael</au><au>Pfrunder‐Cardozo, Katia R.</au><au>Allen, Richard C.</au><au>Hall, Alex R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2020-07</date><risdate>2020</risdate><volume>22</volume><issue>7</issue><spage>2664</spage><epage>2679</epage><pages>2664-2679</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Bacteria in nature often encounter non‐antibiotic antibacterials (NAAs), such as disinfectants and heavy metals, and they can evolve resistance via mechanisms that are also involved in antibiotic resistance. Understanding whether susceptibility to different types of antibacterials is non‐randomly associated across natural and clinical bacteria is therefore important for predicting the spread of resistance, yet there is no consensus about the extent of such associations or underlying mechanisms. We tested for associations between susceptibility phenotypes of 93 natural and clinical Escherichia coli isolates to various NAAs and antibiotics. Across all compound combinations, we detected a small number of non‐random associations, including a trio of positive associations among chloramphenicol, triclosan and benzalkonium chloride. We investigated genetic mechanisms that can explain such associations using genomic information, genetic knockouts and experimental evolution. This revealed some mutations that are selected for by experimental exposure to one compound and confer cross‐resistance to other compounds. Surprisingly, these interactions were asymmetric: selection for chloramphenicol resistance conferred cross‐resistance to triclosan and benzalkonium chloride, but selection for triclosan resistance did not confer cross‐resistance to other compounds. These results identify genetic changes involved in variable cross‐resistance across antibiotics and NAAs, potentially contributing to associations in natural and clinical bacteria.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32162766</pmid><doi>10.1111/1462-2920.14986</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-4158-460X</orcidid><orcidid>https://orcid.org/0000-0002-3654-1373</orcidid><orcidid>https://orcid.org/0000-0001-6012-7888</orcidid><orcidid>https://orcid.org/0000-0001-5909-488X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Antiseptics Bacteria Benzalkonium chloride Benzalkonium Compounds - pharmacology Chloramphenicol Chloramphenicol - pharmacology Chloromycetin Coliforms Disease resistance Disinfectants Disinfectants - pharmacology Drug resistance Drug Resistance, Bacterial - genetics E coli Escherichia coli Escherichia coli - drug effects Escherichia coli - genetics Escherichia coli - isolation & purification Escherichia coli Infections - drug therapy Heavy metals Humans Metals Metals, Heavy - pharmacology Microbial Sensitivity Tests Mutation Phenotypes Triclosan Triclosan - pharmacology |
title | Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli |
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