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Circular intermediate-mediated horizontal transfer of the chromosome-encoded cfr(C) gene in multi-drug resistant Campylobacter coli from swine sources

is a major zoonotic pathogen that causes gastrointestinal and, rarely, immune diseases in humans. The antimicrobial-resistance gene carried by and is a -like gene that targets bacterial 23S rRNA through A2503 methylation. confers cross-resistance to five antimicrobial classes (PhLOPS ), including li...

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Published in:Frontiers in microbiology 2023, Vol.14, p.1274245-1274245
Main Authors: An, Jae-Uk, Lee, Soomin, Guk, Jae-Ho, Woo, Jungha, Song, Hyokeun, Cho, Seongbeom
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Lee, Soomin
Guk, Jae-Ho
Woo, Jungha
Song, Hyokeun
Cho, Seongbeom
description is a major zoonotic pathogen that causes gastrointestinal and, rarely, immune diseases in humans. The antimicrobial-resistance gene carried by and is a -like gene that targets bacterial 23S rRNA through A2503 methylation. confers cross-resistance to five antimicrobial classes (PhLOPS ), including lincosamide, streptogramin A, and pleuromutilin, which are classified as critically important antimicrobials to human by the World Health Organization. To elucidate the genetic variation and horizontal transfer mechanism of , we analyzed the genetic background and horizontal transfer unit of -derived through comparative genomic analysis. We identified nine -positive strains of 157 strains isolated from swine sources. Three novel gene single nucleotide polymorphism (SNP) sites (19delA, 674C > A, and 890 T > C) were identified from nine -positive strains. Among six identified SNP variant types (SNP-I to -VI), five types of randomly inserted -cassettes on chromosome and one type of plasmid-like element were identified, their gene cassette composition differing depending on the variants. Three of six cassette types contained aminoglycoside-streptothricin resistance cluster " - - ." The gene cassette with gene (GC-1, GC-4, and GC-5) formed a -mediated circular intermediate " -hp- - ," which has not been previously reported. Other two cassette-types with ISChh1 formed circular intermediate "ISChh1- - - - - -hp-ATPase" and "ISChh1- - -hp." In conjugation assay, the -mediated circular intermediate was naturally transferred to the plasmid of recipient wild-type strain from swine source, and comparative genomic analysis revealed that encoded in -mediated circular intermediate was inserted into the plasmid of recipient by homologous recombination with and . This study revealed that novel multidrug resistance gene carried by from swine sources can be highly genetically diverse and transferable. Moreover, we suggest that the transferability of chromosomal may contribute to the global spread of multidrug resistance against clinically important antimicrobials.
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The antimicrobial-resistance gene carried by and is a -like gene that targets bacterial 23S rRNA through A2503 methylation. confers cross-resistance to five antimicrobial classes (PhLOPS ), including lincosamide, streptogramin A, and pleuromutilin, which are classified as critically important antimicrobials to human by the World Health Organization. To elucidate the genetic variation and horizontal transfer mechanism of , we analyzed the genetic background and horizontal transfer unit of -derived through comparative genomic analysis. We identified nine -positive strains of 157 strains isolated from swine sources. Three novel gene single nucleotide polymorphism (SNP) sites (19delA, 674C &gt; A, and 890 T &gt; C) were identified from nine -positive strains. Among six identified SNP variant types (SNP-I to -VI), five types of randomly inserted -cassettes on chromosome and one type of plasmid-like element were identified, their gene cassette composition differing depending on the variants. Three of six cassette types contained aminoglycoside-streptothricin resistance cluster " - - ." The gene cassette with gene (GC-1, GC-4, and GC-5) formed a -mediated circular intermediate " -hp- - ," which has not been previously reported. Other two cassette-types with ISChh1 formed circular intermediate "ISChh1- - - - - -hp-ATPase" and "ISChh1- - -hp." In conjugation assay, the -mediated circular intermediate was naturally transferred to the plasmid of recipient wild-type strain from swine source, and comparative genomic analysis revealed that encoded in -mediated circular intermediate was inserted into the plasmid of recipient by homologous recombination with and . This study revealed that novel multidrug resistance gene carried by from swine sources can be highly genetically diverse and transferable. 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The antimicrobial-resistance gene carried by and is a -like gene that targets bacterial 23S rRNA through A2503 methylation. confers cross-resistance to five antimicrobial classes (PhLOPS ), including lincosamide, streptogramin A, and pleuromutilin, which are classified as critically important antimicrobials to human by the World Health Organization. To elucidate the genetic variation and horizontal transfer mechanism of , we analyzed the genetic background and horizontal transfer unit of -derived through comparative genomic analysis. We identified nine -positive strains of 157 strains isolated from swine sources. Three novel gene single nucleotide polymorphism (SNP) sites (19delA, 674C &gt; A, and 890 T &gt; C) were identified from nine -positive strains. Among six identified SNP variant types (SNP-I to -VI), five types of randomly inserted -cassettes on chromosome and one type of plasmid-like element were identified, their gene cassette composition differing depending on the variants. Three of six cassette types contained aminoglycoside-streptothricin resistance cluster " - - ." The gene cassette with gene (GC-1, GC-4, and GC-5) formed a -mediated circular intermediate " -hp- - ," which has not been previously reported. Other two cassette-types with ISChh1 formed circular intermediate "ISChh1- - - - - -hp-ATPase" and "ISChh1- - -hp." In conjugation assay, the -mediated circular intermediate was naturally transferred to the plasmid of recipient wild-type strain from swine source, and comparative genomic analysis revealed that encoded in -mediated circular intermediate was inserted into the plasmid of recipient by homologous recombination with and . This study revealed that novel multidrug resistance gene carried by from swine sources can be highly genetically diverse and transferable. Moreover, we suggest that the transferability of chromosomal may contribute to the global spread of multidrug resistance against clinically important antimicrobials.</description><subject>Campylobacter coli</subject><subject>chromosome-encoded</subject><subject>circular intermediate</subject><subject>horizontal transfer</subject><subject>whole genome sequencing</subject><issn>1664-302X</issn><issn>1664-302X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpNkU1r3DAQhk1paUKaP5BD0TE9eGt92JaOxfQjEOglgdzEWBrtKtjWVpIpyQ_p7602uw3VQTOIeZ8RPFV1RZsN51J9drM344Y1jG8o6wUT7ZvqnHadqHnDHt7-159Vlyk9NuWIhpX7fXXGJZWylfS8-jP4aNYJIvFLxjij9ZCxPlVLdiH657BkmEiOsCSHkQRH8g6J2cUwhxRmrHExwZZp4-L18IlsccHCI_M6ZV_buG5JxORThiWTAeb90xRGMGUfMWHyxBUQSb99SaWwRoPpQ_XOwZTw8lQvqvtvX--GH_Xtz-83w5fb2gjKc42gjGV9B7RVLai-U0aIFqQRI6eSNr21VsFInWxRta6zjorejR1jinUCDL-obo5cG-BR76OfIT7pAF6_PIS41RCzNxNqRRsq0KleyBKVbuSIDZQf9CMfgbvCuj6y9jH8WjFlPftkcJpgwbAmzRSlUhxclVF2HDUxpBTRva6mjT7o1S969UGvPuktoY8n_joWP6-RfzL5X6WypPA</recordid><startdate>2023</startdate><enddate>2023</enddate><creator>An, Jae-Uk</creator><creator>Lee, Soomin</creator><creator>Guk, Jae-Ho</creator><creator>Woo, Jungha</creator><creator>Song, Hyokeun</creator><creator>Cho, Seongbeom</creator><general>Frontiers Media S.A</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>DOA</scope></search><sort><creationdate>2023</creationdate><title>Circular intermediate-mediated horizontal transfer of the chromosome-encoded cfr(C) gene in multi-drug resistant Campylobacter coli from swine sources</title><author>An, Jae-Uk ; Lee, Soomin ; Guk, Jae-Ho ; Woo, Jungha ; Song, Hyokeun ; Cho, Seongbeom</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c413t-ea9cd276a1595a9769c445a8c4b318107ddd9ab1f85e95f6df147fb6229264ac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Campylobacter coli</topic><topic>chromosome-encoded</topic><topic>circular intermediate</topic><topic>horizontal transfer</topic><topic>whole genome sequencing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>An, Jae-Uk</creatorcontrib><creatorcontrib>Lee, Soomin</creatorcontrib><creatorcontrib>Guk, Jae-Ho</creatorcontrib><creatorcontrib>Woo, Jungha</creatorcontrib><creatorcontrib>Song, Hyokeun</creatorcontrib><creatorcontrib>Cho, Seongbeom</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>An, Jae-Uk</au><au>Lee, Soomin</au><au>Guk, Jae-Ho</au><au>Woo, Jungha</au><au>Song, Hyokeun</au><au>Cho, Seongbeom</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Circular intermediate-mediated horizontal transfer of the chromosome-encoded cfr(C) gene in multi-drug resistant Campylobacter coli from swine sources</atitle><jtitle>Frontiers in microbiology</jtitle><addtitle>Front Microbiol</addtitle><date>2023</date><risdate>2023</risdate><volume>14</volume><spage>1274245</spage><epage>1274245</epage><pages>1274245-1274245</pages><issn>1664-302X</issn><eissn>1664-302X</eissn><abstract>is a major zoonotic pathogen that causes gastrointestinal and, rarely, immune diseases in humans. The antimicrobial-resistance gene carried by and is a -like gene that targets bacterial 23S rRNA through A2503 methylation. confers cross-resistance to five antimicrobial classes (PhLOPS ), including lincosamide, streptogramin A, and pleuromutilin, which are classified as critically important antimicrobials to human by the World Health Organization. To elucidate the genetic variation and horizontal transfer mechanism of , we analyzed the genetic background and horizontal transfer unit of -derived through comparative genomic analysis. We identified nine -positive strains of 157 strains isolated from swine sources. Three novel gene single nucleotide polymorphism (SNP) sites (19delA, 674C &gt; A, and 890 T &gt; C) were identified from nine -positive strains. Among six identified SNP variant types (SNP-I to -VI), five types of randomly inserted -cassettes on chromosome and one type of plasmid-like element were identified, their gene cassette composition differing depending on the variants. Three of six cassette types contained aminoglycoside-streptothricin resistance cluster " - - ." The gene cassette with gene (GC-1, GC-4, and GC-5) formed a -mediated circular intermediate " -hp- - ," which has not been previously reported. Other two cassette-types with ISChh1 formed circular intermediate "ISChh1- - - - - -hp-ATPase" and "ISChh1- - -hp." In conjugation assay, the -mediated circular intermediate was naturally transferred to the plasmid of recipient wild-type strain from swine source, and comparative genomic analysis revealed that encoded in -mediated circular intermediate was inserted into the plasmid of recipient by homologous recombination with and . This study revealed that novel multidrug resistance gene carried by from swine sources can be highly genetically diverse and transferable. Moreover, we suggest that the transferability of chromosomal may contribute to the global spread of multidrug resistance against clinically important antimicrobials.</abstract><cop>Switzerland</cop><pub>Frontiers Media S.A</pub><pmid>38188581</pmid><doi>10.3389/fmicb.2023.1274245</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
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subjects Campylobacter coli
chromosome-encoded
circular intermediate
horizontal transfer
whole genome sequencing
title Circular intermediate-mediated horizontal transfer of the chromosome-encoded cfr(C) gene in multi-drug resistant Campylobacter coli from swine sources
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