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Novel integron gene cassette arrays identified in a global collection of multi-drug resistant non-typhoidal Salmonella enterica.

ABSTRACT: Investigation of integron carriage in a global collection of multi-drug resistant Salmonella enterica identified 3 unique class 1 integron gene cassette arrays not previously reported in this species. The present study used PCR and DNA sequence analysis to characterize the structure of these gene cassette arrays. A approximately 4.0 kb integron containing the gene cassette array arr2/cmlA5/bla (OXA10) /aadA1 was found in isolates belonging to serovars Isangi and Typhimurium from South Africa. A approximately 6.0 kb integron containing the gene cassettes aac(6')IIc/ereA2/IS1247/aac/arr/ereA2 was found in isolates belonging to serovar Heidelberg from the Philippines. In this gene cassette array, the insertion sequence, IS1247, and two putative resistance genes, disrupt the erythromycin resistance gene cassette. Finally, a approximately 6.0 kb integron containing the gene cassette qacH/dfrA32/ereA1/aadA2/cmlA/aadA1 was found in serovar Stanley isolates from Taiwan. This integron, which has not been previously reported in any bacterial species, contains a new dihydrofolate reductase gene cassette sequence designated dfrA32, with only 90% sequence similarity to previously reported dfrA cassettes. The S. enterica integrons described in the present study represent novel collections of resistance genes which confer multi-drug resistance and have the potential to be widely disseminated among S. enterica as well as other bacterial species.

SUBMITTER: Krauland M

PROVIDER: S-EPMC2824789 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Novel integron gene cassette arrays identified in a global collection of multi-drug resistant non-typhoidal Salmonella enterica.

Krauland Mary M Harrison Lee L Paterson David D Marsh Jane J

Current microbiology 20100301 3

Investigation of integron carriage in a global collection of multi-drug resistant Salmonella enterica identified 3 unique class 1 integron gene cassette arrays not previously reported in this species. The present study used PCR and DNA sequence analysis to characterize the structure of these gene cassette arrays. A approximately 4.0 kb integron containing the gene cassette array arr2/cmlA5/bla (OXA10) /aadA1 was found in isolates belonging to serovars Isangi and Typhimurium from South Africa. A ...[more]

PMID: 19921331

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Project description:Salmonella enterica serotype Kentucky can be a common causative agent of salmonellosis, usually associated with consumption of contaminated poultry. Antimicrobial resistance (AMR) to multiple drugs, including ciprofloxacin, is an emerging problem within this serotype. We used whole-genome sequencing (WGS) to investigate the phylogenetic structure and AMR content of 121 S.enterica serotype Kentucky sequence type 198 isolates from five continents. Population structure was inferred using phylogenomic analysis and whole genomes were compared to investigate changes in gene content, with a focus on acquired AMR genes. Our analysis showed that multidrug-resistant (MDR) S.enterica serotype Kentucky isolates belonged to a single lineage, which we estimate emerged circa 1989 following the acquisition of the AMR-associated Salmonella genomic island (SGI) 1 (variant SGI1-K) conferring resistance to ampicillin, streptomycin, gentamicin, sulfamethoxazole and tetracycline. Phylogeographical analysis indicates this clone emerged in Egypt before disseminating into Northern, Southern and Western Africa, then to the Middle East, Asia and the European Union. The MDR clone has since accumulated various substitution mutations in the quinolone-resistance-determining regions (QRDRs) of DNA gyrase (gyrA) and DNA topoisomerase IV (parC), such that most strains carry three QRDR mutations which together confer resistance to ciprofloxacin. The majority of AMR genes in the S. enterica serotype Kentucky genomes were carried either on plasmids or SGI structures. Remarkably, each genome of the MDR clone carried a different SGI1-K derivative structure; this variation could be attributed to IS26-mediated insertions and deletions, which appear to have hampered previous attempts to trace the clone's evolution using sub-WGS resolution approaches. Several different AMR plasmids were also identified, encoding resistance to chloramphenicol, third-generation cephalosporins, carbapenems and/or azithromycin. These results indicate that most MDR S. enterica serotype Kentucky circulating globally result from the clonal expansion of a single lineage that acquired chromosomal AMR genes 30 years ago, and has continued to diversify and accumulate additional resistances to last-line oral antimicrobials. This article contains data hosted by Microreact.

Project description:BackgroundIntegrons are genetic elements capable of the acquisition, rearrangement and expression of genes contained in gene cassettes. Gene cassettes generally consist of a promoterless gene associated with a recombination site known as a 59-base element (59-be). Multiple insertion events can lead to the assembly of large integron-associated cassette arrays. The most striking examples are found in Vibrio, where such cassette arrays are widespread and can range from 30 kb to 150 kb. Besides those found in completely sequenced genomes, no such array has yet been recovered in its entirety. We describe an approach to systematically isolate, sequence and annotate large integron gene cassette arrays from bacterial strains.ResultsThe complete Vibrio sp. DAT722 integron cassette array was determined through the streamlined approach described here. To place it in an evolutionary context, we compare the DAT722 array to known vibrio arrays and performed phylogenetic analyses for all of its components (integrase, 59-be sites, gene cassette encoded genes). It differs extensively in terms of genomic context as well as gene cassette content and organization. The phylogenetic tree of the 59-be sites collectively found in the Vibrio gene cassette pool suggests frequent transfer of cassettes within and between Vibrio species, with slower transfer rates between more phylogenetically distant relatives. We also identify multiple cases where non-integron chromosomal genes seem to have been assembled into gene cassettes and others where cassettes have been inserted into chromosomal locations outside integrons.ConclusionOur systematic approach greatly facilitates the isolation and annotation of large integrons gene cassette arrays. Comparative analysis of the Vibrio sp. DAT722 integron obtained through this approach to those found in other vibrios confirms the role of this genetic element in promoting lateral gene transfer and suggests a high rate of gene gain/loss relative to most other loci on vibrio chromosomes. We identify a relationship between the phylogenetic distance separating two species and the rate at which they exchange gene cassettes, interactions between the non-mobile portion of bacterial genomes and the vibrio gene cassette pool as well as intragenomic translocation events of integrons in vibrios.

Project description:BackgroundInvasive Non-typhoidal Salmonella (iNTS) are an important cause of bacteraemia in children and HIV-infected adults in sub-Saharan Africa. Previous research has shown that iNTS strains exhibit a pattern of gene loss that resembles that of host adapted serovars such as Salmonella Typhi and Paratyphi A. Salmonella enterica serovar Bovismorbificans was a common serovar in Malawi between 1997 and 2004.MethodologyWe sequenced the genomes of 14 Malawian bacteraemia and four veterinary isolates from the UK, to identify genomic variations and signs of host adaptation in the Malawian strains.Principal findingsWhole genome phylogeny of invasive and veterinary S. Bovismorbificans isolates showed that the isolates are highly related, belonging to the most common international S. Bovismorbificans Sequence Type, ST142, in contrast to the findings for S. Typhimurium, where a distinct Sequence Type, ST313, is associated with invasive disease in sub-Saharan Africa. Although genome degradation through pseudogene formation was observed in ST142 isolates, there were no clear overlaps with the patterns of gene loss seen in iNTS ST313 isolates previously described from Malawi, and no clear distinction between S. Bovismorbificans isolates from Malawi and the UK. The only defining differences between S. Bovismorbificans bacteraemia and veterinary isolates were prophage-related regions and the carriage of a S. Bovismorbificans virulence plasmid (pVIRBov).ConclusionsiNTS S. Bovismorbificans isolates, unlike iNTS S. Typhiumrium isolates, are only distinguished from those circulating elsewhere by differences in the mobile genome. It is likely that these strains have entered a susceptible population and are able to take advantage of this niche. There are tentative signs of convergent evolution to a more human adapted iNTS variant. Considering its importance in causing disease in this region, S. Bovismorbificans may be at the beginning of this process, providing a reference against which to compare changes that may become fixed in future lineages in sub-Saharan Africa.

Dataset Information

Novel integron gene cassette arrays identified in a global collection of multi-drug resistant non-typhoidal Salmonella enterica.

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Novel integron gene cassette arrays identified in a global collection of multi-drug resistant non-typhoidal Salmonella enterica.

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