Dataset Information

Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid.

ABSTRACT: Salmonella Infantis is one of the five serovars most frequently causing human salmonellosis in Europe, mainly associated with poultry. A clone harbouring a conjugative plasmid of emerging S. Infantis (pESI)-like megaplasmid, carrying multidrug resistant (MDR) and extended-spectrum beta-lactamases (ESBL) genes, has spread in the Italian broiler chicken industry also causing human illness. This work is aimed at elucidating the molecular epidemiology of S. Infantis and pESI-like in Europe using whole-genome sequencing and bioinformatics analysis, and to investigate the genetic relatedness of S. Infantis clones and pESI-like from animals, meat, feed and humans provided by institutions of nine European countries. Two genotyping approaches were used: chromosome or plasmid SNP-based analysis and the minimum spanning tree (MST) algorithm based on core-genome multilocus sequence typing (cgMLST). The European S. Infantis population appeared heterogeneous, with different genetic clusters defined at core-genome level. However, pESI-like variants present in 64.1?% of the isolates were more genetically homogeneous and capable of infecting different clonal lineages in most of the countries. Two different pESI-like with ESBL genes (n=82) were observed: bla CTX-M-1-positive in European isolates and bla CTX-M-65-positive in American isolates (study outgroup). Both variants had toxin-antitoxin systems, resistance genes towards tetracyclines, trimethoprim, sulphonamides and aminoglycosides, heavy metals (merA) and disinfectants (qacE?). Worryingly, 66?% of the total isolates studied presented different gyrA chromosomal point mutations associated with (fluoro)quinolone resistance (MIC range 0.125-0.5?mg/L), while 18?% displayed transferable macrolide resistance mediated by mph, mef and erm(B) genes. Proper intervention strategies are needed to prevent further dissemination/transmission of MDR S. Infantis and pESI-like along the food chain in Europe.

SUBMITTER: Alba P

PROVIDER: S-EPMC7371121 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid.

Alba Patricia P Leekitcharoenphon Pimlapas P Carfora Virginia V Amoruso Roberta R Cordaro Gessica G Di Matteo Paola P Ianzano Angela A Iurescia Manuela M Diaconu Elena L EL Study Group Engage-Eurl-Ar Network EN Pedersen Susanne K SK Guerra Beatriz B Hendriksen Rene S RS Franco Alessia A Battisti Antonio A

Microbial genomics 20200409 5

Salmonella Infantis is one of the five serovars most frequently causing human salmonellosis in Europe, mainly associated with poultry. A clone harbouring a conjugative plasmid of emerging S. Infantis (pESI)-like megaplasmid, carrying multidrug resistant (MDR) and extended-spectrum beta-lactamases (ESBL) genes, has spread in the Italian broiler chicken industry also causing human illness. This work is aimed at elucidating the molecular epidemiology of S. Infantis and pESI-lik ...[more]

PMID: 32271142

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Project description:Salmonella enterica subsp. enterica serovar Infantis is the most prevalent serovar found in broilers and broiler meat and is among the top five serovars responsible for human infections in Europe. In 2008, a multidrug-resistant S. Infantis isolate emerged in Israel with a mosaic megaplasmid named pESI, associated with increased virulence, biofilm formation, and multidrug resistance. Since then, S. Infantis clones with pESI-like plasmids have been reported worldwide, replacing pESI-free clones. Here, we typed 161 S. Infantis isolates of poultry (n = 133) and human clinical (n = 28) origin using whole-genome sequencing. The isolates were collected between 2007 and 2021. In addition, we performed PacBio/Illumina sequencing for two representative pESI-like plasmids and compared them with publicly available sequences. All isolates belonged to sequence type 32 (ST32), except for one isolate that represented a novel single-locus variant of ST32. Core genome MLST (cgMLST) analysis revealed 14 clusters of genetically closely related isolates, of which four suggested broiler-to-human transmission of S. Infantis. pESI-like plasmids were present in 148/161 (91.9%) isolates; all were highly similar to the publicly available pESI-like sequences but lacked extended-spectrum beta-lactamase (ESBL) genes. PacBio/Illumina hybrid assembly allowed the reconstruction of two novel complete pESI variants. The present study revealed that the multidrug-resistant, pESI-positive S. Infantis clone became the predominant S. Infantis clone in Slovenian broilers and humans during the last decade. Continued surveillance of resistant S. Infantis clones along the food chain is needed to guide public health efforts. IMPORTANCE Salmonella Infantis clones with pESI-like plasmids harboring several virulence and resistance genes have been reported worldwide. In the present study, we compared the population structure of 161 Salmonella Infantis isolates obtained from humans and broilers in Slovenia from 2007 to 2021. Whole-genome sequencing showed that most human isolates clustered apart from broiler isolates, suggesting an alternative source of infection. Most isolates were multidrug resistant due to the presence of pESI-like plasmids, of which two variants (pS89 and pS19) were fully reconstructed using long-read sequencing. Both exhibited high similarity with the original Israeli pESI plasmid and German p2747 plasmid. The prototype plasmid pS89 harbored the typical pESI-associated resistance genes aadA1, qacEΔ1, sul1, and tet(A), which were absent in the truncated plasmid pS19.

Project description:Salmonella enterica serovar Infantis is one of the prevalent salmonellae worldwide. Recently, we showed that the emergence of S Infantis in Israel was facilitated by the acquisition of a unique megaplasmid (pESI) conferring multidrug resistance and increased virulence phenotypes. Here we elucidate the ecology, transmission properties, and regulation of pESI. We show that despite its large size (~280 kb), pESI does not impose a significant metabolic burden in vitro and that it has been recently fixed in the domestic S Infantis population. pESI conjugation and the transcription of its pilus (pil) genes are inhibited at the ambient temperature (27°C) and by ≥1% bile but increased under temperatures of 37 to 41°C, oxidative stress, moderate osmolarity, and the microaerobic conditions characterizing the intestinal environment of warm-blooded animals. The pESI-encoded protein TraB and the oxygen homeostasis regulator Fnr were identified as transcriptional regulators of pESI conjugation. Using the mouse model, we show that following S Infantis infection, pESI can be horizontally transferred to the gut microbiota, including to commensal Escherichia coli strains. Possible transfer, but not persistence, of pESI was also observed into Gram-positive mouse microbiota species, especially Lactobacillus reuteri Moreover, pESI was demonstrated to further disseminate from gut microbiota to S. enterica serovar Typhimurium, in the context of gastrointestinal infection. These findings exhibit the ability of a selfish clinically relevant megaplasmid to distribute to and from the microbiota and suggest an overlooked role of the microbiota as a reservoir of mobile genetic elements and intermediator in the spread of resistance and virulence genes between commensals and pathogenic bacteria. Plasmid conjugation plays a key role in microbial evolution, enabling the acquisition of new phenotypes, including resistance and virulence. Salmonella enterica serovar Infantis is one of the ubiquitous salmonellae worldwide and a major cause of foodborne infections. Previously, we showed that the emergence of S Infantis in Israel has involved the acquisition of a unique megaplasmid (pESI) conferring multidrug resistance and increased virulence phenotypes. Recently, the emergence of another S Infantis strain carrying a pESI-like plasmid was identified in Italy, suggesting that the acquisition of pESI may be common to different emergent S Infantis populations globally. Transmission of this plasmid to other strains or bacterial species is an alarming scenario. Understanding the ecology, regulation, and transmission properties of clinically relevant plasmids and the role of the microbiota in their spreading offers a new mechanism explaining the emergence of new pathogenic and resistant biotypes and may assist in the development of appropriate surveillance and prevention measures.

Project description:Recently emerged S. Infantis strains carrying resistance to several commonly used antimicrobials have been reported from different parts of the globe, causing human cases of salmonellosis and with occurrence reported predominantly in broiler chickens. Here, we performed phylogenetic and genetic clustering analyses to describe the population structure of 417 S. Infantis originating from multiple European countries and the Americas collected between 1985 and 2019. Of these, 171 were collected from 56 distinct premises located in England and Wales (E/W) between 2009 and 2019, including isolates linked to incursions of multidrug-resistant (MDR) strains from Europe associated with imported poultry meat. The analysis facilitated the comparison of isolates from different E/W sources with isolates originating from other countries. There was a high degree of congruency between the outputs of different types of population structure analyses revealing that the E/W and central European (Germany, Hungary, and Poland) isolates formed several disparate groups, which were distinct from the cluster relating to the United States (USA) and Ecuador/Peru, but that isolates from Brazil were closely related to the E/W and the central European isolates. Nearly half of the analysed strains/genomes (194/417) harboured the IncFIB(pN55391) replicon typical of the "parasitic" pESI-like megaplasmid found in diverse strains of S. Infantis. The isolates that contained the IncFIB(pN55391) replicon clustered together, despite originating from different parts of the globe. This outcome was corroborated by the time-measured phylogeny, which indicated that the initial acquisition of IncFIB(pN55391) likely occurred in Europe in the late 1980s, with a single introduction of IncFIB(pN55391)-carrying S. Infantis to the Americas several years later. Most of the antimicrobial resistance (AMR) genes were identified in isolates that harboured one or more different plasmids, but based on the short-read assemblies, only a minority of the resistance genes found in these isolates were identified as being associated with the detected plasmids, whereas the hybrid assemblies comprising the short and long reads demonstrated that the majority of the identified AMR genes were associated with IncFIB(pN55391) and other detected plasmid replicon types. This finding underlies the importance of applying appropriate methodologies to investigate associations of AMR genes with bacterial plasmids.

Dataset Information

Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid.

Publications

Molecular epidemiology of <i>Salmonella</i> Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid.

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