Dataset Information

ICE SXT vs. ICESh95: Co-existence of Integrative and Conjugative Elements and Competition for a New Host.

ABSTRACT: Integrative and conjugative elements (ICEs) are mobile genetic elements that contribute to horizontal gene transfer. The aim of this work was to study different types of ICEs in clinical isolates of the emergent pathogen Shewanella spp., to compare their transfer efficiency and their ability to integrate a new host. Here we show that 3 out of 10 clinical isolates contained an ICE. Two of these elements were similar to ICEs from the SXT/R391 family and the other one was similar to ICESh95, a hybrid platform. Mating assays showed that these elements co-exist for several generations in the same host. Furthermore, transfer rates and competition assays between ICESh95 and ICESh392, an SXT-like element, suggest that the latter has evolved into a well-oiled machine that efficiently spread to different bacteria. Our results provide strong evidence of the role that ICEs play in the dissemination of genetic traits in nature and the implications that they have in the global threat of antimicrobial resistance.

SUBMITTER: Parmeciano DI Noto G

PROVIDER: S-EPMC6541609 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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ICE SXT vs. ICESh95: Co-existence of Integrative and Conjugative Elements and Competition for a New Host.

Parmeciano DI Noto Gisela G Iriarte Andrés A Ramírez María Soledad MS Centrón Daniela D Quiroga Cecilia C

Scientific reports 20190529 1

Integrative and conjugative elements (ICEs) are mobile genetic elements that contribute to horizontal gene transfer. The aim of this work was to study different types of ICEs in clinical isolates of the emergent pathogen Shewanella spp., to compare their transfer efficiency and their ability to integrate a new host. Here we show that 3 out of 10 clinical isolates contained an ICE. Two of these elements were similar to ICEs from the SXT/R391 family and the other one was similar to ICESh95, a hybr ...[more]

PMID: 31142760

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Project description:Integrative and conjugative elements (ICEs) of the SXT/R391 family are key drivers of the spread of antibiotic resistance in Vibrio cholerae, the infectious agent of cholera, and other pathogenic bacteria. The SXT/R391 family of ICEs was defined based on the conservation of a core set of 52 genes and site-specific integration into the 5' end of the chromosomal gene prfC Hence, the integrase gene int has been intensively used as a marker to detect SXT/R391 ICEs in clinical isolates. ICEs sharing most core genes but differing by their integration site and integrase gene have been recently reported and excluded from the SXT/R391 family. Here we explored the prevalence and diversity of atypical ICEs in GenBank databases and their relationship with typical SXT/R391 ICEs. We found atypical ICEs in V. cholerae isolates that predate the emergence and expansion of typical SXT/R391 ICEs in the mid-1980s in seventh-pandemic toxigenic V. cholerae strains O1 and O139. Our analyses revealed that while atypical ICEs are not associated with antibiotic resistance genes, they often carry cation efflux pumps, suggesting heavy metal resistance. Atypical ICEs constitute a polyphyletic group likely because of occasional recombination events with typical ICEs. Furthermore, we show that the alternative integration and excision genes of atypical ICEs remain under the control of SetCD, the main activator of the conjugative functions of SXT/R391 ICEs. Together, these observations indicate that substitution of the integration/excision module and change of specificity of integration do not preclude atypical ICEs from inclusion into the SXT/R391 family.IMPORTANCEVibrio cholerae is the causative agent of cholera, an acute intestinal infection that remains to this day a world public health threat. Integrative and conjugative elements (ICEs) of the SXT/R391 family have played a major role in spreading antimicrobial resistance in seventh-pandemic V. cholerae but also in several species of Enterobacteriaceae Most epidemiological surveys use the integrase gene as a marker to screen for SXT/R391 ICEs in clinical or environmental strains. With the recent reports of closely related elements that carry an alternative integrase gene, it became urgent to investigate whether ICEs that have been left out of the family are a liability for the accuracy of such screenings. In this study, based on comparative genomics, we broaden the SXT/R391 family of ICEs to include atypical ICEs that are often associated with heavy metal resistance.

Project description:UNLABELLED:SXT-R391 Integrative conjugative elements (ICEs) are self-transmissible mobile genetic elements able to confer multidrug resistance and other adaptive features to bacterial hosts, including Vibrio cholerae, the causative agent of cholera. ICEs are arranged in a mosaic genetic structure composed of a conserved backbone interspersed with variable DNA clusters located in conserved hot spots. In this study, we investigated ICE acquisition and subsequent microevolution in pandemic V. cholerae. Ninety-six ICEs were retrieved from publicly available sequence databases from V. cholerae clinical strains and were compared to a set of reference ICEs. Comparative genomics highlighted the existence of five main ICE groups with a distinct genetic makeup, exemplified by ICEVchInd5, ICEVchMoz10, SXT, ICEVchInd6, and ICEVchBan11. ICEVchInd5 (the most frequent element, represented by 70 of 96 elements analyzed) displayed no sequence rearrangements and was characterized by 46 single nucleotide polymorphisms (SNPs). SNP analysis revealed that recent inter-ICE homologous recombination between ICEVchInd5 and other ICEs circulating in gammaproteobacteria generated ICEVchMoz10, ICEVchInd6, and ICEVchBan11. Bayesian phylogenetic analyses indicated that ICEVchInd5 and SXT were independently acquired by the current pandemic V. cholerae O1 and O139 lineages, respectively, within a period of only a few years. IMPORTANCE:SXT-R391 ICEs have been recognized as key vectors of antibiotic resistance in the seventh-pandemic lineage of V. cholerae, which remains a major cause of mortality and morbidity on a global scale. ICEs were acquired only recently in this clade and are acknowledged to be major contributors to horizontal gene transfer and the acquisition of new traits in bacterial species. We have reconstructed the temporal dynamics of SXT-R391 ICE acquisition and spread and have identified subsequent recombination events generating significant diversity in ICEs currently circulating among V. cholerae clinical strains. Our results showed that acquisition of SXT-R391 ICEs provided the V. cholerae seventh-pandemic lineage not only with a multidrug resistance phenotype but also with a powerful molecular tool for rapidly accessing the pan-genome of a large number of gammaproteobacteria.

Dataset Information

ICE SXT vs. ICESh95: Co-existence of Integrative and Conjugative Elements and Competition for a New Host.

Publications

ICE SXT vs. ICESh95: Co-existence of Integrative and Conjugative Elements and Competition for a New Host.

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