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. 2019 Jun 21;19(1):132.
doi: 10.1186/s12862-019-1457-5.

Serotype-specific Evolutionary Patterns of Antimicrobial-Resistant Salmonella Enterica

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Free PMC article

Serotype-specific Evolutionary Patterns of Antimicrobial-Resistant Salmonella Enterica

Jingqiu Liao et al. BMC Evol Biol. .
Free PMC article

Abstract

Background: The emergence of antimicrobial-resistant (AMR) strains of the important human and animal pathogen Salmonella enterica poses a growing threat to public health. Here, we studied the genome-wide evolution of 90 S. enterica AMR isolates, representing one host adapted serotype (S. Dublin) and two broad host range serotypes (S. Newport and S. Typhimurium).

Results: AMR S. Typhimurium had a large effective population size, a large and diverse genome, AMR profiles with high diversity, and frequent positive selection and homologous recombination. AMR S. Newport showed a relatively low level of diversity and a relatively clonal population structure. AMR S. Dublin showed evidence for a recent population bottleneck, and the genomes were characterized by a larger number of genes and gene ontology terms specifically absent from this serotype and a significantly higher number of pseudogenes as compared to other two serotypes. Approximately 50% of accessory genes, including specific AMR and putative prophage genes, were significantly over- or under-represented in a given serotype. Approximately 65% of the core genes showed phylogenetic clustering by serotype, including the AMR gene aac (6')-Iaa. While cell surface proteins were shown to be the main target of positive selection, some proteins with possible functions in AMR and virulence also showed evidence for positive selection. Homologous recombination mainly acted on prophage-associated proteins.

Conclusions: Our data indicates a strong association between genome content of S. enterica and serotype. Evolutionary patterns observed in S. Typhimurium are consistent with multiple emergence events of AMR strains and/or ecological success of this serotype in different hosts or habitats. Evolutionary patterns of S. Newport suggested that antimicrobial resistance emerged in one single lineage, Lineage IIC. A recent population bottleneck and genome decay observed in AMR S. Dublin are congruent with its narrow host range. Finally, our results suggest the potentially important role of positive selection in the evolution of antimicrobial resistance, host adaptation and serotype diversification in S. enterica.

Keywords: Antimicrobial resistance; Genome decay; Homologous recombination; Positive selection; Salmonella enterica; Serotypes.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Accumulation curves of a pan genome and b core genome of AMR S. Dublin (in blue), S. Newport (in brown) and S. Typhimurium (in red). The vertical bars indicate the standard deviations based on 100 repetitions with randomization of the order of the genomes
Fig. 2
Fig. 2
Non-metric multidimensional scaling ordination of AMR S. Dublin (in red), S. Newport (in green) and S. Typhimurium (in blue) isolates based on gene presence/absence
Fig. 3
Fig. 3
Bayesian skyline plot indicating changes in the effective population size (Ne) of a AMR S. Dublin, b S. Newport and c S. Typhimurium over time with a relaxed molecular clock. The shaded area represents the 95% confidence intervals
Fig. 4
Fig. 4
The over- and under- representation of a orthologous genes and b GO and EC terms in AMR S. Dublin, S. Newport, and S. Typhimurium. Orthologous genes and GO/EC terms over- / under- represented in one serotype are defined as the ones identified as significant in given comparisons to the other two serotypes (FDR < 0.05, odds ratio >6.71 or < 0.15, respectively, for over- / under- represented)
Fig. 5
Fig. 5
a Phylogenetic tree inferred by maximum likelihood method using the core genome SNPs of 90 S. enterica isolates. Tree is rooted by midpoint. Bootstrap values > 70% are presented on the tree. S. Dublin is indicated by green, S. Newport by blue, and S. Typhimurium by red. b Proportion of core genes with different phylogenetic clustering patterns. Genes showing a phylogenetic clustering by serotype on the tree are indicated in orange. Genes showing phylogenetic clustering of only one serotype (i.e., isolates of one serotype were grouping together while those of other two were not) are indicated in grey. Genes showing no particular clustering pattern are indicated in yellow. Conserved genes (i.e., all sequences were identical) are indicated in blue

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