Dataset Information

Characterization of a fosA3 Carrying IncC-IncN Plasmid From a Multidrug-Resistant ST17 Salmonella Indiana Isolate.

ABSTRACT: The aim of this study was to investigate the characteristics of a fosA3 carrying IncC-IncN plasmid from a multidrug-resistant Salmonella isolate HNK130. HNK130 was isolated from a chicken and identified as ST17 Salmonella enterica serovar Indiana and exhibited resistance to 13 antibiotics including the cephalosporins and fosfomycin. S1 nuclease pulsed-field gel electrophoresis and Southern blot assays revealed that HNK130 harbored only one ?180-kb plasmid carrying fosA3 and bla CTX-M-14, which was not transferable via conjugation. We further examined 107 Escherichia coli electro-transformants and identified 3 different plasmid variants, pT-HNK130-1 (69), pT-HNK130-2 (15), and pT-HNK130-3 (23), in which pT-HNK130-1 seemed to be the same as the plasmid harbored in HNK130. We completely sequenced an example of each of these variants, and all three variants were IncC-IncN multi-incompatible plasmid and showed a mosaic structure. The fosA3 gene was present in all three and bounded by IS26 elements in the same orientation (IS26-322bp-fosA3-1758bp-IS26) that could form a minicircle containing fosA3. The bla CTX-M-14 gene was located within an IS15DI-?IS15DI-iroN-IS903B-bla CTX-M-14 -?ISEcp1-IS26 structure separated from the fosA3 gene in pT-HNK130-1, but was adjacent to fosA3 in pT-HNK130-3 in an inverted orientation. Linear comparison of the three variants showed that pT-HNK130-2 and pT-HNK130-3 resulted from the sequence deletion and inversion of pT-HNK130-1. Stability tests demonstrated that pT-HNK130-1 and pT-HNK130-3 could be stably maintained in the transformants without antibiotic selection but pT-HNK130-2 was unstable. This is the first description of an IncC-IncN hybrid plasmid from an ST17 S. Indiana strain and indicates that this plasmid may further facilitate dissemination of fosfomycin and cephalosporin resistance in Salmonella.

SUBMITTER: Zhang LJ

PROVIDER: S-EPMC7385254 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Characterization of a fosA3 Carrying IncC-IncN Plasmid From a Multidrug-Resistant ST17 Salmonella Indiana Isolate.

Zhang Li-Juan LJ Gu Xi-Xi XX Zhang Jie J Yang Ling L Lu Yue-Wei YW Fang Liang-Xing LX Jiang Hong-Xia HX

Frontiers in microbiology 20200721

The aim of this study was to investigate the characteristics of a fosA3 carrying IncC-IncN plasmid from a multidrug-resistant Salmonella isolate HNK130. HNK130 was isolated from a chicken and identified as ST17 Salmonella enterica serovar Indiana and exhibited resistance to 13 antibiotics including the cephalosporins and fosfomycin. S1 nuclease pulsed-field gel electrophoresis and Southern blot assays revealed that HNK130 harbored only one ∼180-kb plasmid carrying fosA3</ ...[more]

PMID: 32793137

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Project description:Salmonella enterica serovar Indiana (S. Indiana) is an extremely expanded foodborne pathogen in China in recent years. This study aimed to elucidate the national prevalence and phylogenomic characterization of this pathogen in China. Among 5, 287 serotyped Salmonella isolates collected during 2002 to 2018, 466 S. Indiana isolates were found in 15 provinces, and 407 were identified to be ST17, and the rest were ST2040. Among 407 ST17 isolates, 372 (91.4%) were multidrug resistant, and 366 (89.9%) were resistant to ciprofloxacin, 235 (57.7%) were further resistant to ceftriaxone. Phylogenomic analysis revealed that ST17 isolates were classified into four clades (I, II, III and IV), which appeared in international clonal dissemination. ST17 isolates from China fell into Clade IV with part of isolates from the United Kingdom, the United States, South Korea, and Thailand, suggesting their close genetic relationship. Mutations in quinolone resistance-determining regions (QRDR) of GyrA and ParC, and plasmid-mediated quinolone resistance (PMQR) genes aac(6')-Ib-cr, oqxAB, and qnrS as well as extended spectrum β-lactamases (ESBL) genes blaCTX-M, blaOXA, and blaTEM in isolates from Clade IV were much higher than those from other three clades. Various blaCTX-M subtypes (blaCTX-M-65, blaCTX-M-55, blaCTX-M-27, blaCTX-M-14, and blaCTX-M-123) with ISEcp1, IS903B, ISVsa5, and IS1R were found in ST17 isolates, especially Tn1721 containing ΔISEcp1-blaCTX-M-27-IS903B in P1-like bacteriophage plasmids. These findings on the prevalent and genomic characterization for the S. Indiana multidrug-resistant ST17 clone in China, which have not been reported yet, provide valuable insights into the potential risk of this high-resistant clone. IMPORTANCE Fluoroquinolones and cephalosporins are the primary choices for severe salmonellosis treatment. S. Indiana has become one of the most prevalent serovars in breeding poultry and poultry meats in China in recent years. ST17 was recognized as the leading epidemiological importance in S. Indiana because of its high-level resistance to the most of common antibiotics, including ciprofloxacin and ceftriaxone. However, the prevalence and phylogenomic characterization of ST17 isolates are unclear. Here, we did a retrospective screening on a large scale for S. Indiana in China, and performed its phylogenomic analysis. It was found that ST17 isolates had extensive spread in 15 provinces of China and became a multidrug-resistant clone. The international spread of the ST17 isolates was observed among several countries, especially China, the United Kingdom, and the United States. Our study emphasized the importance of surveillance of a high-resistant S. Indiana ST17 clone to combat its threat to public health.

Project description:The genetic features of foodborne Salmonella have changed in recent years as multidrug-resistant (MDR) strains have become prevalent among various serovars. The recent expansion of MDR Salmonella enterica serovar Indiana sequence type 17 (ST17) poses an increasing threat to global public health, as 24.3% (61/251) of S. Indiana isolates in this study exhibited resistance to three clinically important antimicrobial agents: fluoroquinolones (ciprofloxacin), extended-spectrum β-lactams (cephalosporin), and macrolides (azithromycin). Both the evolutionary histories and antimicrobial resistance (AMR) profiles of this serovar remain to be described. Bioinformatic analysis revealed multiple lineages have coexisted and spread throughout China. Specifically, emergence of a predominant lineage appears to be associated with accumulated various substitutions in the chromosomal quinolone resistance-determining regions (GyrA S83F D87N and ParC T57S S80R) (141 [56.2%]), as well as acquisition of an extended-spectrum β-lactamase (ESBL)-producing IncHI2 plasmid that has subsequently undergone extensive rearrangement and an IncX1 plasmid that contains mph(A), conferring resistance to azithromycin. Several other evolutionary events influencing the trajectory of this drug-resistant serovar were also identified, including sporadic acquisitions of blaCTX-M-carrying plasmids, along with chromosomal integration of blaCTX-M within subclusters. Most human isolates reside in clusters containing isolates from animals, mainly from chickens, indicating the close relationship of human isolates with those from food animals. These data demonstrate that MDR S. Indiana ST17 is already widespread and capable of acquiring resistance traits against the clinical important antimicrobial agents, suggesting it should be considered a high-risk global MDR pathogen. The complexity of its evolutionary history has implications for AMR surveillance, epidemiological analysis, and control of emerging clinical lineages. IMPORTANCE The emergence and worldwide spread of AMR Salmonella constitute great public health concerns. S. enterica serovar Indiana is a typical MDR serovar characterized by sporadic reports. However, comprehensive population genomics studies have not been performed on this serovar. This study provides a detailed and comprehensive insight into the rapid evolution of AMR in this important Salmonella serovar in the past 15 years in eight provinces of China. We documented diverse contributory genetic processes, including stable chromosomal integrations of resistance genes, the persistence and evolution of mobile resistance elements within sublineages, and sporadic acquisition of different resistance determinants that occur at all genetic levels (genes, genetic contexts, plasmids, and host strains). There are different mechanisms of antimicrobial resistance in S. enterica serovar Indiana from those of other serovars. This study sheds light on the formation of MDR S. enterica serovar Indiana with chickens as its potential reservoirs and paves the way to curb its further expansion among food animals.

Project description:Salmonella enterica serovar Indiana (S. Indiana) has aroused widespread concern as an important zoonotic pathogen. The molecular mechanism of multidrug resistance (MDR) in S. Indiana is not known and should be assessed. We aim to investigate the molecular mechanism of MDR and the importance of large plasmids carried class 1 integrons in the MDR of foodborne S. Indiana. Class 1 integrons in 48 S. Indiana isolates and 200 isolates of 7 other Salmonella serotypes were detected by polymerase chain reaction (PCR). To analyze the antimicrobial resistance genes (ARGs) of two S. Indiana isolates, designated S. Indiana 15 and S. Indiana 222, next-generation sequencing (NGS) was performed, and the resulting sequences were compared with the complete nucleotide sequences of S. Indiana D90 and S. Indiana C629. Comparative functional analysis was conducted between the intI1 (1,014 bp) of S. Indiana 222 and the intI1 (699 bp) of S. Indiana 15. Plasmid conjugation transfer analysis was performed to analyze the horizontal gene transfer of the integrons-related resistance genes with integron-positive and integron-negative Salmonella isolates. 64.58% of S. Indiana isolates carried class 1 integrons, which was significantly higher than that of other Salmonella serotypes (p < 0.001). The NGS results showed that the S. Indiana 15 and S. Indiana 222 isolates carried a large plasmid with a class 1 integron and multiple ARGs, similar to S. Indiana D90 and S. Indiana C629. Two integrases found in S. Indiana isolates belong to class 1 integrases and could integrate resistance genes into specific integration sites of the integrons. The conjugation frequency of intI1 (1,014 bp) was 6.08 × 10-5, which was significantly higher than that of intI1 (699 bp) (p < 0.01). The large plasmids carrying a class 1 integron and the number of ARGs were strongly correlated (p < 0.001). The conjugation frequency of integron-positive S. Indiana recipient isolates was significantly higher than that of integron-negative recipient isolates (p < 0.05). S. Indiana containing large plasmids carrying a class 1 integron more easily captured resistance genes from other bacteria (S. Enteritidis and S. Derby), which could be an important cause of the emerging pandemic of MDR clones. Graphical abstractS. Indiana containing large plasmids carrying a class 1 integron more easily captured resistance genes from other bacteria (S. Enteritidis and S. Derby), which could be an important cause of the emerging pandemic of MDR clones.

Dataset Information

Characterization of a fosA3 Carrying IncC-IncN Plasmid From a Multidrug-Resistant ST17 Salmonella Indiana Isolate.

Publications

Characterization of a <i>fosA3</i> Carrying IncC-IncN Plasmid From a Multidrug-Resistant ST17 <i>Salmonella</i> Indiana Isolate.

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