Molecular characterization of the integrative and conjugative elements harbouring multidrug resistance genes in Glaesserella parasuis
It is widely known that integrative and conjugative elements (ICEs) play an important role in the transmission of resistance genes and other exogenous genes. The present study aimed to characterize the three novel ICEs including ICEGpa76, ICEGpa44, and ICEGpa11, from Glaesserella parasuis. The ICEs...
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| Veröffentlicht in: | Veterinary microbiology 2024-04, Vol.291, p.110014-110014, Article 110014 |
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| creator | Che, Yongliang Wu, Renjie Li, Hongjie Wang, Longbai Wu, Xuemin Chen, Qiuyong Chen, Rujing Zhou, Lunjiang |
| description | It is widely known that integrative and conjugative elements (ICEs) play an important role in the transmission of resistance genes and other exogenous genes. The present study aimed to characterize the three novel ICEs including ICEGpa76, ICEGpa44, and ICEGpa11, from Glaesserella parasuis. The ICEs from G. parasuis strains d76, Z44, and XP11 were predicted and identified by whole-genome sequencing (WGS) analysis, ICEfinder, and PCR. Characterization of G. parasuis strains carrying ICEs were determined by conjugation assay, antimicrobial susceptibility testing, WGS, phylogenetic analysis, and comparative sequence analysis.The WGS results showed that three ICEs from G. parasuis have a common genetic backbone belonging to characteristics ofthe ICEHpa1 family. The sequence comparison showed that the ICEHpa1 family has five hot spots (HSs) determined by IS6, IS110, and IS256. Moreover, two variable regions (VRs), VR1 and VR2 were determined by multidrug resistance genes and the rearrangement hotspot (rhs) family, respectively. VR1 consists of multidrug resistance genes, ISApl1s, and other accessory genes, while VR2 is composed of IS4, rhs family, transposase, and hypothetical protein genes. Conjugation experiments and MICs revealed that three ICEs could be transferred to G. parasuis strain IV52, indicating these three ICEs could be transmitted horizontally among G. parasuis strains. Additionally, the difference in resistance genes from ICEs might be due to the insertion function of the ISApl1s in VR1, and the rhs family in VR2 might evolve andthen be stably inherited in G. parasuis. These results further elucidated the transmission mechanism of exogenous genes in G. parasuis.
•Three novel ICEs from G. parasuis were identified and characterized in this study.•All the three ICEs contained multidrug-resistance genes.•The ICEGpa11 is the first ICE harboring florfenicol-resistance gene floR in G. parasuis.•The rhs family, as a bacterial toxin, were the first found to exist in the ICEGpa76 and ICEGpa44.•These results further enriched epidemiology of drug-resistance in G. parasuis. |
| doi_str_mv | 10.1016/j.vetmic.2024.110014 |
| format | Article |
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•Three novel ICEs from G. parasuis were identified and characterized in this study.•All the three ICEs contained multidrug-resistance genes.•The ICEGpa11 is the first ICE harboring florfenicol-resistance gene floR in G. parasuis.•The rhs family, as a bacterial toxin, were the first found to exist in the ICEGpa76 and ICEGpa44.•These results further enriched epidemiology of drug-resistance in G. parasuis.</description><identifier>ISSN: 0378-1135</identifier><identifier>EISSN: 1873-2542</identifier><identifier>DOI: 10.1016/j.vetmic.2024.110014</identifier><identifier>PMID: 38335675</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>antibiotic resistance ; family ; Glaesserella (Haemophilus) parasuis ; ICEHpa1 family ; Integrative and conjugative element (ICE) ; microbiology ; Multidrug resistance ; multiple drug resistance ; phylogeny ; rhs family ; sequence analysis ; transposases</subject><ispartof>Veterinary microbiology, 2024-04, Vol.291, p.110014-110014, Article 110014</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c344t-44db2b277c893043674ff84ca75cc610fd983dd40f24ba2e03803ce5f5eaef403</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0378113524000361$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38335675$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Che, Yongliang</creatorcontrib><creatorcontrib>Wu, Renjie</creatorcontrib><creatorcontrib>Li, Hongjie</creatorcontrib><creatorcontrib>Wang, Longbai</creatorcontrib><creatorcontrib>Wu, Xuemin</creatorcontrib><creatorcontrib>Chen, Qiuyong</creatorcontrib><creatorcontrib>Chen, Rujing</creatorcontrib><creatorcontrib>Zhou, Lunjiang</creatorcontrib><title>Molecular characterization of the integrative and conjugative elements harbouring multidrug resistance genes in Glaesserella parasuis</title><title>Veterinary microbiology</title><addtitle>Vet Microbiol</addtitle><description>It is widely known that integrative and conjugative elements (ICEs) play an important role in the transmission of resistance genes and other exogenous genes. The present study aimed to characterize the three novel ICEs including ICEGpa76, ICEGpa44, and ICEGpa11, from Glaesserella parasuis. The ICEs from G. parasuis strains d76, Z44, and XP11 were predicted and identified by whole-genome sequencing (WGS) analysis, ICEfinder, and PCR. Characterization of G. parasuis strains carrying ICEs were determined by conjugation assay, antimicrobial susceptibility testing, WGS, phylogenetic analysis, and comparative sequence analysis.The WGS results showed that three ICEs from G. parasuis have a common genetic backbone belonging to characteristics ofthe ICEHpa1 family. The sequence comparison showed that the ICEHpa1 family has five hot spots (HSs) determined by IS6, IS110, and IS256. Moreover, two variable regions (VRs), VR1 and VR2 were determined by multidrug resistance genes and the rearrangement hotspot (rhs) family, respectively. VR1 consists of multidrug resistance genes, ISApl1s, and other accessory genes, while VR2 is composed of IS4, rhs family, transposase, and hypothetical protein genes. Conjugation experiments and MICs revealed that three ICEs could be transferred to G. parasuis strain IV52, indicating these three ICEs could be transmitted horizontally among G. parasuis strains. Additionally, the difference in resistance genes from ICEs might be due to the insertion function of the ISApl1s in VR1, and the rhs family in VR2 might evolve andthen be stably inherited in G. parasuis. These results further elucidated the transmission mechanism of exogenous genes in G. parasuis.
•Three novel ICEs from G. parasuis were identified and characterized in this study.•All the three ICEs contained multidrug-resistance genes.•The ICEGpa11 is the first ICE harboring florfenicol-resistance gene floR in G. parasuis.•The rhs family, as a bacterial toxin, were the first found to exist in the ICEGpa76 and ICEGpa44.•These results further enriched epidemiology of drug-resistance in G. parasuis.</description><subject>antibiotic resistance</subject><subject>family</subject><subject>Glaesserella (Haemophilus) parasuis</subject><subject>ICEHpa1 family</subject><subject>Integrative and conjugative element (ICE)</subject><subject>microbiology</subject><subject>Multidrug resistance</subject><subject>multiple drug resistance</subject><subject>phylogeny</subject><subject>rhs family</subject><subject>sequence analysis</subject><subject>transposases</subject><issn>0378-1135</issn><issn>1873-2542</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUuLFDEUhYMoTtv6D0SydFNtXlWV2ggy6CiMuNF1SKVuatJUJW0eDePe_22aGl06q0su59wTzofQa0oOlNDu3fFwhrw6c2CEiQOlhFDxBO2o7HnDWsGeoh3hvWwo5e0VepHSkRAiho48R1dcct52fbtDv7-GBUxZdMTmTkdtMkT3S2cXPA4W5zvAzmeYY12dAWs_YRP8sczbGxZYweeEq3cMJTo_47Us2U2xzDhCcilrbwDP4CHVU_hm0ZASRFgWjU81MRWXXqJnVi8JXj3MPfrx6eP368_N7bebL9cfbhvDhciNENPIRtb3Rg6cCN71wlopjO5bYzpK7DRIPk2CWCZGzYBwSbiB1ragwQrC9-jtdvcUw88CKavVJXP5iodQkuK05VSKnj4uZQMTwyC7WvceiU1qYkgpglWn6FYd7xUl6sJKHdXGSl1YqY1Vtb15SCjjCtM_0184VfB-E0Ct5OwgqmQc1DYnF8FkNQX3_4Q_Voqqdg</recordid><startdate>202404</startdate><enddate>202404</enddate><creator>Che, Yongliang</creator><creator>Wu, Renjie</creator><creator>Li, Hongjie</creator><creator>Wang, Longbai</creator><creator>Wu, Xuemin</creator><creator>Chen, Qiuyong</creator><creator>Chen, Rujing</creator><creator>Zhou, Lunjiang</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202404</creationdate><title>Molecular characterization of the integrative and conjugative elements harbouring multidrug resistance genes in Glaesserella parasuis</title><author>Che, Yongliang ; Wu, Renjie ; Li, Hongjie ; Wang, Longbai ; Wu, Xuemin ; Chen, Qiuyong ; Chen, Rujing ; Zhou, Lunjiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c344t-44db2b277c893043674ff84ca75cc610fd983dd40f24ba2e03803ce5f5eaef403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>antibiotic resistance</topic><topic>family</topic><topic>Glaesserella (Haemophilus) parasuis</topic><topic>ICEHpa1 family</topic><topic>Integrative and conjugative element (ICE)</topic><topic>microbiology</topic><topic>Multidrug resistance</topic><topic>multiple drug resistance</topic><topic>phylogeny</topic><topic>rhs family</topic><topic>sequence analysis</topic><topic>transposases</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Che, Yongliang</creatorcontrib><creatorcontrib>Wu, Renjie</creatorcontrib><creatorcontrib>Li, Hongjie</creatorcontrib><creatorcontrib>Wang, Longbai</creatorcontrib><creatorcontrib>Wu, Xuemin</creatorcontrib><creatorcontrib>Chen, Qiuyong</creatorcontrib><creatorcontrib>Chen, Rujing</creatorcontrib><creatorcontrib>Zhou, Lunjiang</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Veterinary microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Che, Yongliang</au><au>Wu, Renjie</au><au>Li, Hongjie</au><au>Wang, Longbai</au><au>Wu, Xuemin</au><au>Chen, Qiuyong</au><au>Chen, Rujing</au><au>Zhou, Lunjiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular characterization of the integrative and conjugative elements harbouring multidrug resistance genes in Glaesserella parasuis</atitle><jtitle>Veterinary microbiology</jtitle><addtitle>Vet Microbiol</addtitle><date>2024-04</date><risdate>2024</risdate><volume>291</volume><spage>110014</spage><epage>110014</epage><pages>110014-110014</pages><artnum>110014</artnum><issn>0378-1135</issn><eissn>1873-2542</eissn><abstract>It is widely known that integrative and conjugative elements (ICEs) play an important role in the transmission of resistance genes and other exogenous genes. The present study aimed to characterize the three novel ICEs including ICEGpa76, ICEGpa44, and ICEGpa11, from Glaesserella parasuis. The ICEs from G. parasuis strains d76, Z44, and XP11 were predicted and identified by whole-genome sequencing (WGS) analysis, ICEfinder, and PCR. Characterization of G. parasuis strains carrying ICEs were determined by conjugation assay, antimicrobial susceptibility testing, WGS, phylogenetic analysis, and comparative sequence analysis.The WGS results showed that three ICEs from G. parasuis have a common genetic backbone belonging to characteristics ofthe ICEHpa1 family. The sequence comparison showed that the ICEHpa1 family has five hot spots (HSs) determined by IS6, IS110, and IS256. Moreover, two variable regions (VRs), VR1 and VR2 were determined by multidrug resistance genes and the rearrangement hotspot (rhs) family, respectively. VR1 consists of multidrug resistance genes, ISApl1s, and other accessory genes, while VR2 is composed of IS4, rhs family, transposase, and hypothetical protein genes. Conjugation experiments and MICs revealed that three ICEs could be transferred to G. parasuis strain IV52, indicating these three ICEs could be transmitted horizontally among G. parasuis strains. Additionally, the difference in resistance genes from ICEs might be due to the insertion function of the ISApl1s in VR1, and the rhs family in VR2 might evolve andthen be stably inherited in G. parasuis. These results further elucidated the transmission mechanism of exogenous genes in G. parasuis.
•Three novel ICEs from G. parasuis were identified and characterized in this study.•All the three ICEs contained multidrug-resistance genes.•The ICEGpa11 is the first ICE harboring florfenicol-resistance gene floR in G. parasuis.•The rhs family, as a bacterial toxin, were the first found to exist in the ICEGpa76 and ICEGpa44.•These results further enriched epidemiology of drug-resistance in G. parasuis.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>38335675</pmid><doi>10.1016/j.vetmic.2024.110014</doi><tpages>1</tpages></addata></record> |
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| subjects | antibiotic resistance family Glaesserella (Haemophilus) parasuis ICEHpa1 family Integrative and conjugative element (ICE) microbiology Multidrug resistance multiple drug resistance phylogeny rhs family sequence analysis transposases |
| title | Molecular characterization of the integrative and conjugative elements harbouring multidrug resistance genes in Glaesserella parasuis |
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