Sara Domingues, Tiago Lima, Corentin Escobar, Julie Plantade, Xavier Charpentier, Gabriela Jorge da Silva
{"title":"在自然转化过程中,isec9介导的大DNA片段转位允许抗微生物抗性基因在种间传播。","authors":"Sara Domingues, Tiago Lima, Corentin Escobar, Julie Plantade, Xavier Charpentier, Gabriela Jorge da Silva","doi":"10.1007/s10096-025-05113-9","DOIUrl":null,"url":null,"abstract":"<p><strong>Purpose: </strong>Antimicrobial resistance poses a significant global health challenge, contributing to a lack of effective therapeutic agents, especially against Gram-negative bacteria. Resistance dissemination is accelerated by horizontal gene transfer (HGT) mechanisms. The extended-spectrum beta lactamases CTX-M confer resistance to several beta-lactams, are usually embedded into plasmids and thought to be mainly disseminated by conjugation. However, an increasing number of isolates carry these enzyme-encoding genes in the chromosome, suggesting that they can spread by other means of HGT. In this study, we aimed to test the involvement of natural transformation in the chromosomal acquisition of a bla<sub>CTX-M</sub> gene.</p><p><strong>Methods: </strong>Natural transformation assays were performed during motility on wet surfaces. Acquisition of foreign DNA by transformants was screened by antimicrobial susceptibility testing, polymerase-chain reaction (PCR) and whole genome sequencing (WGS).</p><p><strong>Results: </strong>Acinetobacter baumannii A118, a naturally competent clinical strain, was transformed with naked DNA from Salmonella enterica serovar Typhimurium Sal25, which was isolated from swine meat. The transformation occurred at low frequency (2.7 × 10<sup>- 8</sup> ± 2.04 × 10<sup>- 8</sup> transformants per recipient) and bla<sub>CTX-M</sub> was acquired in one transformant, which was named ACI. WGS of the transformant revealed the acquisition of the bla<sub>CTX-M-32</sub> as part of a ca. 36 Kb DNA fragment through an ISEc9-mediated transposition event; various mobile genetic elements and other resistance genes were co-transferred. The bla<sub>CTX-M-32</sub> gene was subsequently transferred within A. baumannii at a higher frequency (1.8 × 10<sup>- 6</sup> ± 2.49 × 10<sup>- 6</sup> transformants per recipient).</p><p><strong>Conclusion: </strong>Our results highlight the importance of natural transformation events in the dissemination of antimicrobial resistance genes and mobile genetic elements between and within species.</p>","PeriodicalId":11782,"journal":{"name":"European Journal of Clinical Microbiology & Infectious Diseases","volume":" ","pages":"1417-1424"},"PeriodicalIF":3.7000,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12116815/pdf/","citationCount":"0","resultStr":"{\"title\":\"Large DNA fragment ISEc9-mediated transposition during natural transformation allows interspecies dissemination of antimicrobial resistance genes.\",\"authors\":\"Sara Domingues, Tiago Lima, Corentin Escobar, Julie Plantade, Xavier Charpentier, Gabriela Jorge da Silva\",\"doi\":\"10.1007/s10096-025-05113-9\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Purpose: </strong>Antimicrobial resistance poses a significant global health challenge, contributing to a lack of effective therapeutic agents, especially against Gram-negative bacteria. Resistance dissemination is accelerated by horizontal gene transfer (HGT) mechanisms. The extended-spectrum beta lactamases CTX-M confer resistance to several beta-lactams, are usually embedded into plasmids and thought to be mainly disseminated by conjugation. However, an increasing number of isolates carry these enzyme-encoding genes in the chromosome, suggesting that they can spread by other means of HGT. In this study, we aimed to test the involvement of natural transformation in the chromosomal acquisition of a bla<sub>CTX-M</sub> gene.</p><p><strong>Methods: </strong>Natural transformation assays were performed during motility on wet surfaces. Acquisition of foreign DNA by transformants was screened by antimicrobial susceptibility testing, polymerase-chain reaction (PCR) and whole genome sequencing (WGS).</p><p><strong>Results: </strong>Acinetobacter baumannii A118, a naturally competent clinical strain, was transformed with naked DNA from Salmonella enterica serovar Typhimurium Sal25, which was isolated from swine meat. The transformation occurred at low frequency (2.7 × 10<sup>- 8</sup> ± 2.04 × 10<sup>- 8</sup> transformants per recipient) and bla<sub>CTX-M</sub> was acquired in one transformant, which was named ACI. WGS of the transformant revealed the acquisition of the bla<sub>CTX-M-32</sub> as part of a ca. 36 Kb DNA fragment through an ISEc9-mediated transposition event; various mobile genetic elements and other resistance genes were co-transferred. The bla<sub>CTX-M-32</sub> gene was subsequently transferred within A. baumannii at a higher frequency (1.8 × 10<sup>- 6</sup> ± 2.49 × 10<sup>- 6</sup> transformants per recipient).</p><p><strong>Conclusion: </strong>Our results highlight the importance of natural transformation events in the dissemination of antimicrobial resistance genes and mobile genetic elements between and within species.</p>\",\"PeriodicalId\":11782,\"journal\":{\"name\":\"European Journal of Clinical Microbiology & Infectious Diseases\",\"volume\":\" \",\"pages\":\"1417-1424\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2025-06-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12116815/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"European Journal of Clinical Microbiology & Infectious Diseases\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1007/s10096-025-05113-9\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/3/28 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q2\",\"JCRName\":\"INFECTIOUS DISEASES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"European Journal of Clinical Microbiology & Infectious Diseases","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1007/s10096-025-05113-9","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/3/28 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
Large DNA fragment ISEc9-mediated transposition during natural transformation allows interspecies dissemination of antimicrobial resistance genes.
Purpose: Antimicrobial resistance poses a significant global health challenge, contributing to a lack of effective therapeutic agents, especially against Gram-negative bacteria. Resistance dissemination is accelerated by horizontal gene transfer (HGT) mechanisms. The extended-spectrum beta lactamases CTX-M confer resistance to several beta-lactams, are usually embedded into plasmids and thought to be mainly disseminated by conjugation. However, an increasing number of isolates carry these enzyme-encoding genes in the chromosome, suggesting that they can spread by other means of HGT. In this study, we aimed to test the involvement of natural transformation in the chromosomal acquisition of a blaCTX-M gene.
Methods: Natural transformation assays were performed during motility on wet surfaces. Acquisition of foreign DNA by transformants was screened by antimicrobial susceptibility testing, polymerase-chain reaction (PCR) and whole genome sequencing (WGS).
Results: Acinetobacter baumannii A118, a naturally competent clinical strain, was transformed with naked DNA from Salmonella enterica serovar Typhimurium Sal25, which was isolated from swine meat. The transformation occurred at low frequency (2.7 × 10- 8 ± 2.04 × 10- 8 transformants per recipient) and blaCTX-M was acquired in one transformant, which was named ACI. WGS of the transformant revealed the acquisition of the blaCTX-M-32 as part of a ca. 36 Kb DNA fragment through an ISEc9-mediated transposition event; various mobile genetic elements and other resistance genes were co-transferred. The blaCTX-M-32 gene was subsequently transferred within A. baumannii at a higher frequency (1.8 × 10- 6 ± 2.49 × 10- 6 transformants per recipient).
Conclusion: Our results highlight the importance of natural transformation events in the dissemination of antimicrobial resistance genes and mobile genetic elements between and within species.
期刊介绍:
EJCMID is an interdisciplinary journal devoted to the publication of communications on infectious diseases of bacterial, viral and parasitic origin.