Polyphyletic Nature of Salmonella enterica Serotype Derby and Lineage-Specific Host-Association Revealed by Genome-Wide Analysis

Abstract

In France, Salmonella Derby is one of the most prevalent serotypes in pork and poultry meat. Since 2006, it has ranked among the 10 most frequent Salmonella serotypes isolated in humans. In previous publications, Salmonella Derby isolates have been characterized by pulsed field gel electrophoresis (PFGE) and antimicrobial resistance (AMR) profiles revealing the existence of different pulsotypes and AMR phenotypic groups. However, these results suffer from the low discriminatory power of these typing methods. In the present study, we built a collection of 140 strains of S. Derby collected in France from 2014 to 2015 representative of the pork and poultry food sectors. The whole collection was characterized using whole genome sequencing (WGS), providing a significant contribution to the knowledge of this underrepresented serotype, with few genomes available in public databases. The genetic diversity of the S. Derby strains was analyzed by single-nucleotide polymorphism (SNP). We also investigated AMR by both genome and phenotype, the main Salmonella pathogenicity island (SPI) and the fimH gene sequences. Our results show that this S. Derby collection is spread across four different lineages genetically distant by an average of 15k SNPs. These lineages correspond to four multilocus sequence typing (MLST) types (ST39, ST40, ST71, and ST682), which were found to be associated with specific animal hosts: pork and poultry. While the ST71 and ST682 strains are pansusceptible, ST40 isolates are characterized by the multidrug resistant profile STR-SSS-TET. Considering virulence determinants, only ST39 and ST40 present the SPI-23, which has previously been associated with pork enterocyte invasion. Furthermore, the pork ST682 isolates were found to carry mutations in the fimH sequence that could participate in the host tropism of this group. Our phylogenetic analysis demonstrates the polyphyletic nature of the Salmonella serotype Derby and provides an opportunity to identify genetic factors associated with host adaptation and markers for the monitoring of these different lineages within the corresponding animal sectors. The recognition of these four lineages is of primary importance for epidemiological surveillance throughout the food production chains and constitutes the first step toward refining monitoring and preventing dispersal of this pathogen.

Worldwide Epidemiology ofSalmonellaSerovars in Animal-Based Foods: a Meta-analysis

“…Moreover, several studies have demonstrated correlations between S. Derby in pigs and humans (80,(82)(83)(84)(85)(86)(87). For example, in Italy, a comparison of the pulsed-field gel electrophoresis (PFGE) profiles of swine and human isolates confirmed a strong correlation between S. Derby isolated from animals in slaughterhouses and those held at lairage for long periods.…”

Identifying emerging trends in antimicrobial resistance using Salmonella surveillance data in poultry in Spain

“…Derby, the most prevalent serotype in the panel, and presented a MDR phenotype. Previous studies have suggested that this serotype, commonly found in pig and poultry, is polyphyletic, with certain lineages being primarily recovered from either pig or poultry (Hayward, Petrovska, Jansen, & Woodward, ; Sevellec et al, ). Interestingly, typing of 140 isolates representative of the pork and poultry food sectors in France retrieved in 2014–2015 revealed that while MDR phenotypes (with resistance to amynoglycosides, sulphonamides and tetracycline) were associated with pig‐specific lineages in France, isolates from poultry were typically pansusceptible (Sevellec et al, ).…”

Whole genome sequencing and metagenomics for outbreak investigation, source attribution and risk assessment of food‐borne microorganisms

“…Databases rely on proper serotyping from providing laboratories. Bioinformatic resources are required to analyse WGS data, including analysis pipelines for assembly, annotation, and interpretation of the data, which will require a coordinated international approach (Franz et al., ; Oulas et al., ). Novel O‐ and H‐types continue to be identified, especially for STEC, and there is a requirement for continued database up‐dating and curation for Salmonella and STEC. WGS O‐ and H‐antigen data can be used to define new serotypes that do not match ‘classically defined’ serotypes. WGS‐inferred serotypes can in most instances be compared directly with classical serotyping data ensuring comparability of results between laboratories working following different methods. If WGS‐inferred serotypes of Salmonella and STEC are collected centrally in a timely way, these data could form the basis for a powerful first level detection of clusters in outbreak investigations and source tracing. Identification of subgroups within Salmonella serotypes and discrimination among lineages of polyphyletic serotypes can provide insights into host specificity (Sévellec et al., ). With WGS, control surveillance could be focused on the pathotype concept for STEC considering virulence genes instead of serogroup/serotype (sero‐/pathotype).…”

“…Thus, interpretation of WGS data has to consider the knowledge of the natural mutation rates of the particular pathogen, and its behaviour in the food chain under the specific environmental processing factors (e.g. temperature, pH value, pressure, disinfection procedures) (Besser et al, 2018;Sch € urch et al, 2018). In consequence, this might lead to misinterpretation when epidemiological data of the samples are not sufficiently considered.…”