Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: Insights from cell membrane, enzyme, energy supply and transcriptomics
The abuse of antibiotics on animals could induce the development of antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB), and acesulfame potassium (ACE) is the widely used artificial sweetener in animal feed. Generally speaking, ACE and ARB often coexist in livestock wastewater,...
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Veröffentlicht in: | Journal of hazardous materials 2022-01, Vol.422, p.126942-126942, Article 126942 |
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creator | Li, Ziqiao Gao, Jingfeng Guo, Yi Cui, Yingchao Wang, Yuwei Duan, Wanjun Wu, Zejie |
description | The abuse of antibiotics on animals could induce the development of antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB), and acesulfame potassium (ACE) is the widely used artificial sweetener in animal feed. Generally speaking, ACE and ARB often coexist in livestock wastewater, however, the impact of the co-occurrence of ACE and ARB on the transmission of ARGs is still unknown. In this study, the effects of ACE on vertical gene transfer (VGT) and horizontal gene transfer (HGT) were both evaluated. For VGT, ACE may hinder the spread of sul gene in Pseudomonas HLS-6 by blocking ARB growth. As for HGT (from Escherichia coli DH5α to Pseudomonas HLS-6), environmentally relevant ACE concentration could facilitate the conjugative transfer. The underlying mechanisms of HGT were characterized by enhanced cell membrane permeability, reactive oxygen species overproduction, SOS response, energy supply, which were all further verified by the changes in transcription levels of related genes. Interestingly, intracellular Mg2+ in donor strain was found for the first time as an indicator for the conjugation occurrence in ACE treated mating system. This study may provide new insights into the role of ACE on ARGs proliferation and highlight its potential environmental impacts.
[Display omitted]
•Environment-relevant level ACE could facilitate ARGs spread, while higher not.•Increased membrane permeability in donor played a crucial role in conjugation.•Conjugation induced by ACE occurred with enhanced oxidative stress.•Intracellular Mg2+ change in donor strain was a good indicator for conjugation.•ACE above 40.2 mg/L inhibited the VGT of ARGs by blocking ARB growth. |
doi_str_mv | 10.1016/j.jhazmat.2021.126942 |
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[Display omitted]
•Environment-relevant level ACE could facilitate ARGs spread, while higher not.•Increased membrane permeability in donor played a crucial role in conjugation.•Conjugation induced by ACE occurred with enhanced oxidative stress.•Intracellular Mg2+ change in donor strain was a good indicator for conjugation.•ACE above 40.2 mg/L inhibited the VGT of ARGs by blocking ARB growth.</description><identifier>ISSN: 0304-3894</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2021.126942</identifier><identifier>PMID: 34449343</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Acesulfame potassium ; Angiotensin Receptor Antagonists ; Angiotensin-Converting Enzyme Inhibitors ; Animals ; Anti-Bacterial Agents - toxicity ; Cell Membrane ; Drug Resistance, Microbial ; Gene Transfer, Horizontal ; Genes, Bacterial ; Horizontal gene transfer ; Intracellular Mg2 ; Reactive oxygen species ; Sweetening Agents - toxicity ; Thiazines ; Transcriptome ; Vertical gene transfer</subject><ispartof>Journal of hazardous materials, 2022-01, Vol.422, p.126942-126942, Article 126942</ispartof><rights>2021 Elsevier B.V.</rights><rights>Copyright © 2021 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c365t-6718cfca1bf41688f235ce1723aaa8b7c2bddbe86d4cb258417c6035ed9d3b6b3</citedby><cites>FETCH-LOGICAL-c365t-6718cfca1bf41688f235ce1723aaa8b7c2bddbe86d4cb258417c6035ed9d3b6b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jhazmat.2021.126942$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34449343$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Ziqiao</creatorcontrib><creatorcontrib>Gao, Jingfeng</creatorcontrib><creatorcontrib>Guo, Yi</creatorcontrib><creatorcontrib>Cui, Yingchao</creatorcontrib><creatorcontrib>Wang, Yuwei</creatorcontrib><creatorcontrib>Duan, Wanjun</creatorcontrib><creatorcontrib>Wu, Zejie</creatorcontrib><title>Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: Insights from cell membrane, enzyme, energy supply and transcriptomics</title><title>Journal of hazardous materials</title><addtitle>J Hazard Mater</addtitle><description>The abuse of antibiotics on animals could induce the development of antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB), and acesulfame potassium (ACE) is the widely used artificial sweetener in animal feed. Generally speaking, ACE and ARB often coexist in livestock wastewater, however, the impact of the co-occurrence of ACE and ARB on the transmission of ARGs is still unknown. In this study, the effects of ACE on vertical gene transfer (VGT) and horizontal gene transfer (HGT) were both evaluated. For VGT, ACE may hinder the spread of sul gene in Pseudomonas HLS-6 by blocking ARB growth. As for HGT (from Escherichia coli DH5α to Pseudomonas HLS-6), environmentally relevant ACE concentration could facilitate the conjugative transfer. The underlying mechanisms of HGT were characterized by enhanced cell membrane permeability, reactive oxygen species overproduction, SOS response, energy supply, which were all further verified by the changes in transcription levels of related genes. Interestingly, intracellular Mg2+ in donor strain was found for the first time as an indicator for the conjugation occurrence in ACE treated mating system. This study may provide new insights into the role of ACE on ARGs proliferation and highlight its potential environmental impacts.
[Display omitted]
•Environment-relevant level ACE could facilitate ARGs spread, while higher not.•Increased membrane permeability in donor played a crucial role in conjugation.•Conjugation induced by ACE occurred with enhanced oxidative stress.•Intracellular Mg2+ change in donor strain was a good indicator for conjugation.•ACE above 40.2 mg/L inhibited the VGT of ARGs by blocking ARB growth.</description><subject>Acesulfame potassium</subject><subject>Angiotensin Receptor Antagonists</subject><subject>Angiotensin-Converting Enzyme Inhibitors</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - toxicity</subject><subject>Cell Membrane</subject><subject>Drug Resistance, Microbial</subject><subject>Gene Transfer, Horizontal</subject><subject>Genes, Bacterial</subject><subject>Horizontal gene transfer</subject><subject>Intracellular Mg2</subject><subject>Reactive oxygen species</subject><subject>Sweetening Agents - toxicity</subject><subject>Thiazines</subject><subject>Transcriptome</subject><subject>Vertical gene transfer</subject><issn>0304-3894</issn><issn>1873-3336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctuEzEUhkcIRNPCI4C8ZEGCb-OZsEGoKqVSJTawtnw50zga24OPB5S-EK_JhAS2rP7F-c5NX9O8YnTDKFPv9pv9zjxGUzeccrZhXG0lf9KsWN-JtRBCPW1WVFC5Fv1WXjSXiHtKKeta-by5EFLKrZBi1fy6STuTHERIleSBmFSDDbkGRwpgwHosEh8QIYZkasiJ2AMxpYYhuGBGgj8BKiQoxDjAeRxMBDLlahDDHN-Tu4ThYVeRDCVH4mAcSYRoi0nwlkB6PMQ_CeXhQHCepnGZnjypC4CuhKnmGBy-aJ4NZkR4ec6r5tunm6_Xn9f3X27vrj_er51QbV2rjvVucIbZQTLV9wMXrQPWcWGM6W3nuPXeQq-8dJa3vWSdU1S04LdeWGXFVfPmNHcq-fsMWHUMeDx6OTfPqHmrFOV924oFbU-oKxmxwKCnEqIpB82oPjrSe312pI-O9MnR0vf6vGK2Efy_rr9SFuDDCYDl0R8BikYXYPHgQwFXtc_hPyt-AyTnq0Y</recordid><startdate>20220115</startdate><enddate>20220115</enddate><creator>Li, Ziqiao</creator><creator>Gao, Jingfeng</creator><creator>Guo, Yi</creator><creator>Cui, Yingchao</creator><creator>Wang, Yuwei</creator><creator>Duan, Wanjun</creator><creator>Wu, Zejie</creator><general>Elsevier B.V</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>7X8</scope></search><sort><creationdate>20220115</creationdate><title>Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: Insights from cell membrane, enzyme, energy supply and transcriptomics</title><author>Li, Ziqiao ; Gao, Jingfeng ; Guo, Yi ; Cui, Yingchao ; Wang, Yuwei ; Duan, Wanjun ; Wu, Zejie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c365t-6718cfca1bf41688f235ce1723aaa8b7c2bddbe86d4cb258417c6035ed9d3b6b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Acesulfame potassium</topic><topic>Angiotensin Receptor Antagonists</topic><topic>Angiotensin-Converting Enzyme Inhibitors</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - toxicity</topic><topic>Cell Membrane</topic><topic>Drug Resistance, Microbial</topic><topic>Gene Transfer, Horizontal</topic><topic>Genes, Bacterial</topic><topic>Horizontal gene transfer</topic><topic>Intracellular Mg2</topic><topic>Reactive oxygen species</topic><topic>Sweetening Agents - toxicity</topic><topic>Thiazines</topic><topic>Transcriptome</topic><topic>Vertical gene transfer</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Ziqiao</creatorcontrib><creatorcontrib>Gao, Jingfeng</creatorcontrib><creatorcontrib>Guo, Yi</creatorcontrib><creatorcontrib>Cui, Yingchao</creatorcontrib><creatorcontrib>Wang, Yuwei</creatorcontrib><creatorcontrib>Duan, Wanjun</creatorcontrib><creatorcontrib>Wu, Zejie</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of hazardous materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Ziqiao</au><au>Gao, Jingfeng</au><au>Guo, Yi</au><au>Cui, Yingchao</au><au>Wang, Yuwei</au><au>Duan, Wanjun</au><au>Wu, Zejie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: Insights from cell membrane, enzyme, energy supply and transcriptomics</atitle><jtitle>Journal of hazardous materials</jtitle><addtitle>J Hazard Mater</addtitle><date>2022-01-15</date><risdate>2022</risdate><volume>422</volume><spage>126942</spage><epage>126942</epage><pages>126942-126942</pages><artnum>126942</artnum><issn>0304-3894</issn><eissn>1873-3336</eissn><abstract>The abuse of antibiotics on animals could induce the development of antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB), and acesulfame potassium (ACE) is the widely used artificial sweetener in animal feed. Generally speaking, ACE and ARB often coexist in livestock wastewater, however, the impact of the co-occurrence of ACE and ARB on the transmission of ARGs is still unknown. In this study, the effects of ACE on vertical gene transfer (VGT) and horizontal gene transfer (HGT) were both evaluated. For VGT, ACE may hinder the spread of sul gene in Pseudomonas HLS-6 by blocking ARB growth. As for HGT (from Escherichia coli DH5α to Pseudomonas HLS-6), environmentally relevant ACE concentration could facilitate the conjugative transfer. The underlying mechanisms of HGT were characterized by enhanced cell membrane permeability, reactive oxygen species overproduction, SOS response, energy supply, which were all further verified by the changes in transcription levels of related genes. Interestingly, intracellular Mg2+ in donor strain was found for the first time as an indicator for the conjugation occurrence in ACE treated mating system. This study may provide new insights into the role of ACE on ARGs proliferation and highlight its potential environmental impacts.
[Display omitted]
•Environment-relevant level ACE could facilitate ARGs spread, while higher not.•Increased membrane permeability in donor played a crucial role in conjugation.•Conjugation induced by ACE occurred with enhanced oxidative stress.•Intracellular Mg2+ change in donor strain was a good indicator for conjugation.•ACE above 40.2 mg/L inhibited the VGT of ARGs by blocking ARB growth.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>34449343</pmid><doi>10.1016/j.jhazmat.2021.126942</doi><tpages>1</tpages></addata></record> |
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subjects | Acesulfame potassium Angiotensin Receptor Antagonists Angiotensin-Converting Enzyme Inhibitors Animals Anti-Bacterial Agents - toxicity Cell Membrane Drug Resistance, Microbial Gene Transfer, Horizontal Genes, Bacterial Horizontal gene transfer Intracellular Mg2 Reactive oxygen species Sweetening Agents - toxicity Thiazines Transcriptome Vertical gene transfer |
title | Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: Insights from cell membrane, enzyme, energy supply and transcriptomics |
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