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Stability, entrapment and variant formation of Salmonella genomic island 1.

ABSTRACT: BACKGROUND: The Salmonella genomic island 1 (SGI1) is a 42.4 kb integrative mobilizable element containing several antibiotic resistance determinants embedded in a complex integron segment In104. The numerous SGI1 variants identified so far, differ mainly in this segment and the explanations of their emergence were mostly based on comparative structure analyses. Here we provide experimental studies on the stability, entrapment and variant formation of this peculiar gene cluster originally found in S. Typhimurium. METHODOLOGY/PRINCIPAL FINDINGS: Segregation and conjugation tests and various molecular techniques were used to detect the emerging SGI1 variants in Salmonella populations of 17 Salmonella enterica serovar Typhimurium DT104 isolates from Hungary. The SGI1s in these isolates proved to be fully competent in excision, conjugal transfer by the IncA/C helper plasmid R55, and integration into the E. coli chromosome. A trap vector has been constructed and successfully applied to capture the island on a plasmid. Monitoring of segregation of SGI1 indicated high stability of the island. SGI1-free segregants did not accumulate during long-term propagation, but several SGI1 variants could be obtained. Most of them appeared to be identical to SGI1-B and SGI1-C, but two new variants caused by deletions via a short-homology-dependent recombination process have also been detected. We have also noticed that the presence of the conjugation helper plasmid increased the formation of these deletion variants considerably. CONCLUSIONS/SIGNIFICANCE: Despite that excision of SGI1 from the chromosome was proven in SGI1(+)Salmonella populations, its complete loss could not be observed. On the other hand, we demonstrated that several variants, among them two newly identified ones, arose with detectable frequencies in these populations in a short timescale and their formation was promoted by the helper plasmid. This reflects that IncA/C helper plasmids are not only involved in the horizontal spreading of SGI1, but may also contribute to its evolution.

SUBMITTER: Kiss J

PROVIDER: S-EPMC3285670 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Stability, entrapment and variant formation of Salmonella genomic island 1.

Kiss János J Nagy Béla B Olasz Ferenc F

PloS one 20120223 2

<h4>Background</h4>The Salmonella genomic island 1 (SGI1) is a 42.4 kb integrative mobilizable element containing several antibiotic resistance determinants embedded in a complex integron segment In104. The numerous SGI1 variants identified so far, differ mainly in this segment and the explanations of their emergence were mostly based on comparative structure analyses. Here we provide experimental studies on the stability, entrapment and variant formation of this peculiar gene cluster originally ...[more]

PMID: 22384263

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Project description:Salmonella enterica serovar Kentucky ST198 is a major health threat due to its resistance to ciprofloxacin and several other drugs, including third-generation cephalosporins. Many drug-resistant genes have been identified in the Salmonella genomic island 1 variant K (SGI1-K). In this study, we investigated the antimicrobial resistance (AMR) profile and genotypic relatedness of two isolates of ciprofloxacin-resistant (CIPR) S. Kentucky ST198 from poultry in Northeastern Thailand. We successfully assembled the complete genomes of both isolates, namely SSSE-01 and SSSE-03, using hybrid de novo assembly of both short- and long-read sequence data. The complete genomes revealed their highly similar genomic structures and a novel variant of SGI1-K underlying multidrug-resistant (MDR) patterns, including the presence of blaTEM-1b, which confers resistance to beta-lactams, including cephalosporins and lnu(F) which confers resistance to lincomycin and other lincosamides. In addition, the chromosomal mutations in the quinolone resistance-determining region (QRDR) were found at positions 83 (Ser83Phe) and 87 (Asp87Asn) of GyrA and at positions 57 (Thr57Ser) and 80 (Ser80Ile) of ParC suggesting high resistance to ciprofloxacin. We also compared SSSE-01 and SSSE-03 with publicly available complete genome data and revealed significant variations in SGI1-K genetic structures and variable relationships to antibiotic resistance. In comparison to the other isolates, SGI1-K of SSSE-01 and SSSE-03 had a relatively large deletion in the backbone, spanning from S011 (traG∆) to S027 (resG), and the inversion of the IS26-S044∆-yidY segment. Their MDR region was characterized by the inversion of a large segment, including the mer operon and the relocation of IntI1 and several resistance genes downstream of the IS26-S044∆-yidY segment. These structural changes were likely mediated by the recombination of IS26. The findings broaden our understanding of the possible evolution pathway of SGI1-K in fostering drug resistance, which may provide opportunities to control these MDR strains.IMPORTANCEThe emergence of ciprofloxacin-resistant (CIPR) Salmonella Kentucky ST198 globally has raised significant concerns. This study focuses on two poultry isolates from Thailand, revealing a distinct Salmonella genomic island 1 variant K (SGI1-K) genetic structure. Remarkably, multiple antibiotic resistance genes (ARGs) were identified within the SGI1-K as well as other locations in the chromosome, but not in plasmids. Comparing the SGI1-K genetic structures among global and even within-country isolates unveiled substantial variations. Intriguingly, certain isolates lacked ARGs within the SGI1-K, while others had ARGs relocated outside. The presence of chromosomal extended-spectrum β-lactamase (ESBL) genes and lincosamide resistance, lnu(F), gene, could potentially inform the choices of the treatment of CIPRS. Kentucky ST198 infections in humans. This study highlights the importance of understanding the diverse genetic structures of SGI1-K and emphasizes the role of animals and humans in the emergence of antimicrobial resistance.

Project description:Salmonella genomic island 1 (SGI1) is an integrative genetic island first described in Salmonella enterica serovars Typhimurium DT104 and Agona in 2000. Variants of it have since been described in multiple serovars of S. enterica, as well as in Proteus mirabilis, Acinetobacter baumannii, Morganella morganii, and several other genera. The island typically confers resistance to older, first-generation antimicrobials; however, some variants carry blaNDM-1, blaVEB-6, and blaCTX-M15 genes that encode resistance to frontline, clinically important antibiotics, including third-generation cephalosporins. Genome sequencing studies of avian pathogenic Escherichia coli (APEC) identified a sequence type 117 (ST117) isolate (AVC96) with genetic features found in SGI1. The complete genome sequence of AVC96 was assembled from a combination of Illumina and single-molecule real-time (SMRT) sequence data. Analysis of the AVC96 chromosome identified a variant of SGI1-B located 18 bp from the 3' end of trmE, also known as the attB site, a known hot spot for the integration of genomic islands. This is the first report of SGI1 in wild-type E. coli The variant, here named SGI1-B-Ec1, was otherwise unremarkable, apart from the identification of ISEc43 in open reading frame (ORF) S023.IMPORTANCE SGI1 and variants of it carry a variety of antimicrobial resistance genes, including those conferring resistance to extended-spectrum β-lactams and carbapenems, and have been found in diverse S. enterica serovars, Acinetobacter baumannii, and other members of the Enterobacteriaceae SGI1 integrates into Gram-negative pathogenic bacteria by targeting a conserved site 18 bp from the 3' end of trmE For the first time, we describe a novel variant of SGI1 in an avian pathogenic Escherichia coli isolate. The presence of SGI1 in E. coli is significant because it represents yet another lateral gene transfer mechanism to enhancing the capacity of E. coli to acquire and propagate antimicrobial resistance and putative virulence genes. This finding underscores the importance of whole-genome sequencing (WGS) to microbial genomic epidemiology, particularly within a One Health context. Further studies are needed to determine how widespread SGI1 and variants of it may be in Australia.

Dataset Information

Stability, entrapment and variant formation of Salmonella genomic island 1.

Publications

Stability, entrapment and variant formation of Salmonella genomic island 1.

Similar Datasets

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