Genomic diversity and antimicrobial resistance among non-typhoidal Salmonella associated with human disease in The Gambia
Saffiatou DarboeRichard S. BradburyJody PhelanAbdoulie KantehAbdul Khalie MuhammadArchibald WorwuiShangxin YangDavis NwakanmaBlanca M. Perez-SepulvedaSamuel KariukiBrenda Kwambana-AdamsMartín Antonio
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Abstract Non-typhoidal Salmonella associated with multidrug resistance cause invasive disease in sub-Saharan African. Specific lineages of serovars S . Typhimurium and S . Enteritidis are implicated. We characterised the genomic diversity of 100 clinical Non-typhoidal Salmonella collected from 93 patients in 2001 from the eastern and 2006 to 2018 in the western regions of The Gambia respectively. Phenotypic susceptibility applied Kirby Baur disk diffusion and whole genome sequencing utilized Illumina platforms. The predominant serovars were S. Typhimurium ST19 (31/100) and S. Enteritidis ST11 (18/100) restricted to invasive disease with the notable absence of S. Typhimurium ST313. Phylogenetic analysis performed in the context of 495 African strains from the European Nucleotide Archive confirmed the presence of the S . Enteritidis virulent epidemic invasive multidrug resistant West African clade. Multidrug resistance including chloramphenicol and azithromycin has emerged among the West African S. Enteritidis clade 7/9 (78%) with potential for spread, thus having important implications for patient management warranting systematic surveillance and epidemiologic investigations to inform control. Data summary Sequences are deposited in the NCBI sequence reads archive (SRA) under BioProject ID:PRJEB38968. The genomic assemblies are available for download from the European Nucleotide Archive (ENA): http://www.ebi.ac.uk/ena/data/view/ . Accession numbers SAMEA6991082 to SAME6991180Keywords:
Salmonella enteritidis
Genomic island
Salmonella enterica
Multilocus sequence typing
ABSTRACT Salmonella genomic island 3 (SGI3) was first described as a chromosomal island in Salmonella 4,[5],12:i:-, a monophasic variant of Salmonella enterica subsp. enterica serovar Typhimurium. The SGI3 DNA sequence detected from Salmonella 4,[5],12:i:-isolated in Japan was identical to that of a previously reported one across entire length of 81 kb. SGI3 consists of 86 open reading frames, including a copper homeostasis and silver resistance island (CHASRI) and an arsenic resistance operon in addition to genes related to conjugative transfer and DNA replication or partitioning, suggesting that the island is a mobile genetic element. We successfully selected transconjugants that acquired SGI3 after filter mating experiments using the S. enterica serovars Typhimurium, Heidelberg, Hadar, Newport, Cerro, and Thompson as recipients. Southern blot analysis using I-CeuI-digested genomic DNA demonstrated that SGI3 was integrated into a chromosomal fragment of the transconjugants. PCR and sequencing analysis demonstrated that SGI3 was inserted into the 3′ end of the tRNA genes pheV or pheR . The length of the target site was 52 or 55 bp, and a 55-bp attI sequence indicating generation of the circular form of SGI3 was also detected. The transconjugants had a higher MIC against CuSO 4 compared with the recipient strains under anaerobic conditions. Resistance was defined by the cus gene cluster in the CHASRI. The transconjugants also had distinctly higher MICs against Na 2 HAsO 4 compared with recipient strains under aerobic conditions. These findings clearly demonstrate that SGI3 is an integrative and conjugative element and contributes to the copper and arsenic resistance of S. enterica .
Salmonella enterica
Genomic island
genomic DNA
Pathogenicity island
Southern blot
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Multiple-antibiotic-resistant Salmonella enterica serotype Typhimurium is a food-borne pathogen that may be more virulent than related strains lacking the multiresistance phenotype. Salmonella enterica serotype Typhimurium phage type DT104 is the most prevalent of these multiresistant/hypervirulent strains. Multiresistance in DT104 is conferred by an integron structure, designated Salmonella genomic island 1 (SGI1), while we recently demonstrated DT104 hyperinvasion mediated by rumen protozoa (RPz) that are normal flora of cattle. Hyperinvasion was also observed in other Salmonella strains, i.e., other S. enterica serovar Typhimurium phage types and other S. enterica serovars, like S. enterica serovar Infantis, possessing SGI1, while DT104 strains lacking SGI1 were not hyperinvasive. Herein we attempted to identify SGI1 genes involved in the RPz-mediated hyperinvasion of Salmonella strains bearing SGI1. Transposon mutagenesis, coupled with a novel reporter system, revealed the involvement of an SGI1 gene previously designated SO13. Disruption of SO13 expression led to an abrogation of hyperinvasion as assessed by tissue culture invasion assays and by bovine challenge experiments. However, hyperinvasion was not observed in non-SGI1-bearing strains of Salmonella engineered to express SO13. That is, SO13 and another SGI1 gene(s) may coordinately upregulate invasion in DT104 exposed to RPz.
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Salmonella enterica is a foodborne pathogen of significant public health concern worldwide. In Thailand, S. enterica has also been ranked among the top five most significant bacterial agents of foodborne illnesses by the Ministry of Public Health. Conventionally, biochemical tests and antigen-antibody agglutination have been used to identify and subtype S. enterica, respectively. The objective of this study was to identify the serotypes of 180 S. enterica isolates. Multilocus sequence typing (MLST) was used to deduce the S. enterica serotypes based on sequence type (ST) correlation as shown in the MLST database (http://mlst.warwick.ac.uk/mlst/). Initially, MLST was used to confirm serotypes of 53 previously identified isolates of S. Enteritidis, S. Typhimurium, S. Hadar, S. Virchow, and S. Infantis isolated in Thailand. MLST and serotype correlation confirmed 52 (of 53) known isolates. MLST was performed in 127 S. enterica isolates of unknown serotypes from various sources. Serotypes of all 127 S. enterica isolates were successfully deduced based on STs. With MLST and PCR-based identification, we have shown that the majority of isolates are of monophasic S. Typhimurium (ST34; 43 isolates) and serotype Rissen (ST469; 37 isolates), in agreement with the top serotypes commonly found in Thailand based on the WHO National Salmonella and Shigella Center. We have also confirmed that MLST is a powerful Salmonella subtyping method which could be used not only as a tracking tool for an outbreak investigation at nucleotide level but also as a serotype predictor for making correlations with food safety regulations.
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Subtyping
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The fourth mobile sulfonamide resistance gene sul4 has been discovered in many metagenomic datasets. However, there is no reports of it in cultured bacteria. In this study, a sul4 positive clinical Salmonella enterica SC2020597 was obtained by conventional Salmonella isolation methods and characterized by species identification and antimicrobial susceptibility testing. Meanwhile, the genomic DNA was sequenced using both long-read and short-read methods. Following that, the complete genome was analyzed by bioinformatic methods. The sul4 gene in S. enterica SC2020597 differed from the sul4 identified in metagenomic data by one amino acid and could confer full resistance to sulfamethoxazole. Genetic location analysis showed that the sul4 in SC2020597 was carried by a complex chromosomally integrated hybrid plasmid. IS CR20 -like was strongly associated with the mobilization of sul4 by core genetic context analysis. To the best of our knowledge, this is the first report of the emergence of sul4 in clinically cultured S. enterica . More important, the sul4 has the potential to spread to other bacteria with the help of mobile elements.
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Sulfonamide
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Multidrug-resistant Salmonella enterica isolates are an increasing problem worldwide; nevertheless, the mechanisms responsible for such resistance are rarely well defined. Multidrug-resistant S. enterica serovar Typhimurium isolates ST3224 and ST827 were collected from two patients.
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The multi-antimicrobial resistance gene cluster and its derivatives have been detected in Salmonella genomic island 1 (SGI1), which has been identified in the Salmonella enterica serovar Typhimurium, phage types DT104, DT12, DT120, and U302, as well as other Salmonella serovars, including Agona, Paratyphi B, Albany, Meleagridis, Newport, Cerro, Derby, Dusseldorf, Infantis, Kiambu, and Emek. We acquired 53 Salmonella Typhimurium DT104 isolates from diarrheal patients in Korea. From these isolates, we identified a novel antimicrobial resistance gene cluster as an additional gene cassette in SGI1 from a multi-antimicrobial resistant isolate. The minimum inhibitory concentration for this isolate against ampicillin and chloramphenicol was two to four times higher than those for other multi-antimicrobial–resistant Salmonella Typhimurium DT104 isolates. The new antimicrobial resistance gene cluster detected in this isolate consisted of blaPSE-1, sul1Δ, floR, and tetR, in that order. The order of this gene cluster was shuffled as compared to that of the known In104 in SGI1. This report is, to the best of our knowledge, the first to identify and describe an additional shuffled antimicrobial resistance gene cluster in SGI1.
Salmonella enterica
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Gene cluster
Human pathogen
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Salmonella genomic island 3 (SGI3) was first described as a chromosomal island in Salmonella 4,[5],12:i:-, a monophasic variant of Salmonella enterica subsp. enterica serovar Typhimurium. The SGI3 DNA sequence detected from Salmonella 4,[5],12:i:- isolated in Japan was identical to that of a previously reported one across entire length of 81 kb. SGI3 consists of 86 open reading frames, including a copper homeostasis and silver resistance island (CHASRI) and an arsenic tolerance operon, in addition to genes related to conjugative transfer and DNA replication or partitioning, suggesting that the island is a mobile genetic element. We successfully selected transconjugants that acquired SGI3 after filter-mating experiments using the S. enterica serovars Typhimurium, Heidelberg, Hadar, Newport, Cerro, and Thompson as recipients. Southern blot analysis using I-CeuI-digested genomic DNA demonstrated that SGI3 was integrated into a chromosomal fragment of the transconjugants. PCR and sequencing analysis demonstrated that SGI3 was inserted into the 3' end of the tRNA genes pheV or pheR The length of the target site was 52 or 55 bp, and a 55-bp attI sequence indicating generation of the circular form of SGI3 was also detected. The transconjugants had a higher MIC against CuSO4 compared to the recipient strains under anaerobic conditions. Tolerance was defined by the cus gene cluster in the CHASRI. The transconjugants also had distinctly higher MICs against Na2HAsO4 compared to recipient strains under aerobic conditions. These findings clearly demonstrate that SGI3 is an integrative and conjugative element and contributes to the copper and arsenic tolerance of S. enterica.
Salmonella enterica
Genomic island
Pathogenicity island
genomic DNA
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Salmonella enterica
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The global dissemination of the multiply-antibiotic-resistant Salmonella enterica serovar Typhimurium DT104 clone with the resistance genes located in a class 1 integron, here designated In104, within genomic island SGI1 is a significant public health issue. Here, we have shown that SGI1 and variants of it carrying different combinations of resistance genes are found in several Salmonella enterica serovars. These are serovars Cerro, Derby, Dusseldorf, Infantis, Kiambu, and Paratyphi B dT(+) isolated from human infections and serovar Emek from sewage effluent. Two new variants, SGI1-I and SGI1-J, both of which include the dfrA1-orfC cassette array, were identified.
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Genomic island
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Objectives: To determine the prevalence of integron-mediated antibiotic resistance in a diverse sample set of Salmonella enterica isolated from animals.
Salmonella enterica
Genomic island
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