Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli
This study investigated the potential role of phages in the dissemination of antimicrobial resistance genes (ARGs) and virulence factor genes (VFGs) in Escherichia coli (E. coli). A comprehensive in silico analysis of 18,410 phage sequences retrieved from the National Center for Biotechnology Inform...
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description | This study investigated the potential role of phages in the dissemination of antimicrobial resistance genes (ARGs) and virulence factor genes (VFGs) in Escherichia coli (E. coli). A comprehensive in silico analysis of 18,410 phage sequences retrieved from the National Center for Biotechnology Information database (NCBI) revealed distinct carriage patterns for ARGs and VFGs between lytic, temperate, and chronic phage types. Notably, 57 temperate phages carried ARGs, particularly associated with multidrug and aminoglycoside resistance. Temperate phages (8.97 %, 635/7081) and chronic phages (8.09 %, 14/173) exhibited a significantly higher prevalence of VFGs (Chi-Square, p ≤ 0.05), particularly associated with exotoxin-related genes, compared to lytic phages (0.05 %, 6/11,156). This underscores the role phages play as reservoirs and potential vectors for the dissemination of ARGs and VFGs in bacteria. Our environmental E. coli isolates (n = 60) were found to carry 179 intact prophages containing polymyxin, macrolide, tetracycline, and multidrug resistance genes as well as various VFGs. This study documents the presence of phage-plasmids (P-Ps) in environmental E. coli isolates, offering new insights into horizontal gene transfer (HGT) mechanisms. Notably, the blaCTX-M-15 gene, associated with beta-lactam resistance, was identified in two P-Ps, suggesting a potentially novel route for the dissemination of beta-lactam resistance. The diverse replicon types observed in P-Ps suggest a broader integration capacity compared to traditional plasmids, potentially enabling the blaCTX-M-15 gene dissemination across diverse bacterial species. This study provides valuable insights into the multifaceted role of phages in shaping the antimicrobial resistance landscape. Further research is necessary to fully understand the intricate mechanisms underlying phage-mediated ARG and VFG dissemination.
[Display omitted]
•Temperate phages carried more ARGs and VFGs than lytic phages.•Chronic phage primarily carried exotoxin VFGs.•Environmental E. coli isolates carried prophages with ARGs and VFGs.•Phage-plasmid (P-Ps) potentially contributes to ARG and VFG dissemination.•Identified blaCTX-M-15 within P-Ps, suggesting a novel pathway for dissemination |
doi_str_mv | 10.1016/j.scitotenv.2024.178157 |
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[Display omitted]
•Temperate phages carried more ARGs and VFGs than lytic phages.•Chronic phage primarily carried exotoxin VFGs.•Environmental E. coli isolates carried prophages with ARGs and VFGs.•Phage-plasmid (P-Ps) potentially contributes to ARG and VFG dissemination.•Identified blaCTX-M-15 within P-Ps, suggesting a novel pathway for dissemination</description><identifier>ISSN: 0048-9697</identifier><identifier>ISSN: 1879-1026</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.178157</identifier><identifier>PMID: 39729844</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Anti-Bacterial Agents - pharmacology ; Antimicrobial resistance gene ; Bacteriophages - genetics ; Bacteriophages - physiology ; Bioinformatics ; Drug Resistance, Bacterial - genetics ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Phage ; Phage genomics ; Phage-plasmid ; Plasmids - genetics ; Virulence factor gene ; Virulence Factors - genetics</subject><ispartof>The Science of the total environment, 2025-01, Vol.959, p.178157, Article 178157</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1624-507f98398b921e9a68004d27d3e52f87d87bdf57fbbbaddbb0f3c78412ccaae3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0048969724083153$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39729844$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ku, H.</creatorcontrib><creatorcontrib>Kelk, D.</creatorcontrib><creatorcontrib>Bauer, D.C.</creatorcontrib><creatorcontrib>Sidhu, J.P.S.</creatorcontrib><title>Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli</title><title>The Science of the total environment</title><addtitle>Sci Total Environ</addtitle><description>This study investigated the potential role of phages in the dissemination of antimicrobial resistance genes (ARGs) and virulence factor genes (VFGs) in Escherichia coli (E. coli). A comprehensive in silico analysis of 18,410 phage sequences retrieved from the National Center for Biotechnology Information database (NCBI) revealed distinct carriage patterns for ARGs and VFGs between lytic, temperate, and chronic phage types. Notably, 57 temperate phages carried ARGs, particularly associated with multidrug and aminoglycoside resistance. Temperate phages (8.97 %, 635/7081) and chronic phages (8.09 %, 14/173) exhibited a significantly higher prevalence of VFGs (Chi-Square, p ≤ 0.05), particularly associated with exotoxin-related genes, compared to lytic phages (0.05 %, 6/11,156). This underscores the role phages play as reservoirs and potential vectors for the dissemination of ARGs and VFGs in bacteria. Our environmental E. coli isolates (n = 60) were found to carry 179 intact prophages containing polymyxin, macrolide, tetracycline, and multidrug resistance genes as well as various VFGs. This study documents the presence of phage-plasmids (P-Ps) in environmental E. coli isolates, offering new insights into horizontal gene transfer (HGT) mechanisms. Notably, the blaCTX-M-15 gene, associated with beta-lactam resistance, was identified in two P-Ps, suggesting a potentially novel route for the dissemination of beta-lactam resistance. The diverse replicon types observed in P-Ps suggest a broader integration capacity compared to traditional plasmids, potentially enabling the blaCTX-M-15 gene dissemination across diverse bacterial species. This study provides valuable insights into the multifaceted role of phages in shaping the antimicrobial resistance landscape. Further research is necessary to fully understand the intricate mechanisms underlying phage-mediated ARG and VFG dissemination.
[Display omitted]
•Temperate phages carried more ARGs and VFGs than lytic phages.•Chronic phage primarily carried exotoxin VFGs.•Environmental E. coli isolates carried prophages with ARGs and VFGs.•Phage-plasmid (P-Ps) potentially contributes to ARG and VFG dissemination.•Identified blaCTX-M-15 within P-Ps, suggesting a novel pathway for dissemination</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antimicrobial resistance gene</subject><subject>Bacteriophages - genetics</subject><subject>Bacteriophages - physiology</subject><subject>Bioinformatics</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - genetics</subject><subject>Phage</subject><subject>Phage genomics</subject><subject>Phage-plasmid</subject><subject>Plasmids - genetics</subject><subject>Virulence factor gene</subject><subject>Virulence Factors - genetics</subject><issn>0048-9697</issn><issn>1879-1026</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkMtuGzEMRYWgRewm-YVWy27GlTQPSUvDyKNAgHaRZQBBD05MY2bkSmMD_vvKcJptueHmkJc8hHzjbMUZ737sVtnjHGeYjivBRLPiUvFWXpElV1JXnInuE1ky1qhKd1ouyJecd6xUwa7JotZSaNU0S_L6e2vfoNoPNo8Y6PbkEoZMbaZH8HNMmfYxUTvN6DDO6GmCjHm2kweKEy35mOI0wjTbgd5nv4WEfouW-jjgLfnc2yHD3Xu_IS8P9y-bp-r51-PPzfq58rwTTdUy2WtVa-W04KBtp8rhQchQQyt6JYOSLvSt7J1zNgTnWF97qRouvLcW6hvy_bJ2n-KfA-TZjJg9DIOdIB6yqXmjZatExwoqL6hPMecEvdknHG06Gc7M2azZmQ-z5mzWXMyWya_vIQc3QviY-6eyAOsLAOXTI0I6L4LiKWAqKk2I-N-Qv78JkMI</recordid><startdate>20250110</startdate><enddate>20250110</enddate><creator>Ku, H.</creator><creator>Kelk, D.</creator><creator>Bauer, D.C.</creator><creator>Sidhu, J.P.S.</creator><general>Elsevier B.V</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope></search><sort><creationdate>20250110</creationdate><title>Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli</title><author>Ku, H. ; Kelk, D. ; Bauer, D.C. ; Sidhu, J.P.S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1624-507f98398b921e9a68004d27d3e52f87d87bdf57fbbbaddbb0f3c78412ccaae3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antimicrobial resistance gene</topic><topic>Bacteriophages - genetics</topic><topic>Bacteriophages - physiology</topic><topic>Bioinformatics</topic><topic>Drug Resistance, Bacterial - genetics</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - genetics</topic><topic>Phage</topic><topic>Phage genomics</topic><topic>Phage-plasmid</topic><topic>Plasmids - genetics</topic><topic>Virulence factor gene</topic><topic>Virulence Factors - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ku, H.</creatorcontrib><creatorcontrib>Kelk, D.</creatorcontrib><creatorcontrib>Bauer, D.C.</creatorcontrib><creatorcontrib>Sidhu, J.P.S.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ku, H.</au><au>Kelk, D.</au><au>Bauer, D.C.</au><au>Sidhu, J.P.S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2025-01-10</date><risdate>2025</risdate><volume>959</volume><spage>178157</spage><pages>178157-</pages><artnum>178157</artnum><issn>0048-9697</issn><issn>1879-1026</issn><eissn>1879-1026</eissn><abstract>This study investigated the potential role of phages in the dissemination of antimicrobial resistance genes (ARGs) and virulence factor genes (VFGs) in Escherichia coli (E. coli). A comprehensive in silico analysis of 18,410 phage sequences retrieved from the National Center for Biotechnology Information database (NCBI) revealed distinct carriage patterns for ARGs and VFGs between lytic, temperate, and chronic phage types. Notably, 57 temperate phages carried ARGs, particularly associated with multidrug and aminoglycoside resistance. Temperate phages (8.97 %, 635/7081) and chronic phages (8.09 %, 14/173) exhibited a significantly higher prevalence of VFGs (Chi-Square, p ≤ 0.05), particularly associated with exotoxin-related genes, compared to lytic phages (0.05 %, 6/11,156). This underscores the role phages play as reservoirs and potential vectors for the dissemination of ARGs and VFGs in bacteria. Our environmental E. coli isolates (n = 60) were found to carry 179 intact prophages containing polymyxin, macrolide, tetracycline, and multidrug resistance genes as well as various VFGs. This study documents the presence of phage-plasmids (P-Ps) in environmental E. coli isolates, offering new insights into horizontal gene transfer (HGT) mechanisms. Notably, the blaCTX-M-15 gene, associated with beta-lactam resistance, was identified in two P-Ps, suggesting a potentially novel route for the dissemination of beta-lactam resistance. The diverse replicon types observed in P-Ps suggest a broader integration capacity compared to traditional plasmids, potentially enabling the blaCTX-M-15 gene dissemination across diverse bacterial species. This study provides valuable insights into the multifaceted role of phages in shaping the antimicrobial resistance landscape. Further research is necessary to fully understand the intricate mechanisms underlying phage-mediated ARG and VFG dissemination.
[Display omitted]
•Temperate phages carried more ARGs and VFGs than lytic phages.•Chronic phage primarily carried exotoxin VFGs.•Environmental E. coli isolates carried prophages with ARGs and VFGs.•Phage-plasmid (P-Ps) potentially contributes to ARG and VFG dissemination.•Identified blaCTX-M-15 within P-Ps, suggesting a novel pathway for dissemination</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39729844</pmid><doi>10.1016/j.scitotenv.2024.178157</doi><oa>free_for_read</oa></addata></record> |
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subjects | Anti-Bacterial Agents - pharmacology Antimicrobial resistance gene Bacteriophages - genetics Bacteriophages - physiology Bioinformatics Drug Resistance, Bacterial - genetics Escherichia coli - drug effects Escherichia coli - genetics Phage Phage genomics Phage-plasmid Plasmids - genetics Virulence factor gene Virulence Factors - genetics |
title | Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli |
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