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.2023 Oct 3;6(1):1007.
doi: 10.1038/s42003-023-05365-1.

Multidrug resistance plasmids underlie clonal expansions and international spread of Salmonella enterica serotype 1,4,[5],12:i:- ST34 in Southeast Asia

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Multidrug resistance plasmids underlie clonal expansions and international spread of Salmonella enterica serotype 1,4,[5],12:i:- ST34 in Southeast Asia

Hao Chung The et al. Commun Biol..

Abstract

Salmonella enterica serotype 1,4,[5],12:i:- (Typhimurium monophasic variant) of sequence type (ST) 34 has emerged as the predominant pandemic genotype in recent decades. Despite increasing reports of resistance to antimicrobials in Southeast Asia, Salmonella ST34 population structure and evolution remained understudied in the region. Here we performed detailed genomic investigations on 454 ST34 genomes collected from Vietnam and diverse geographical sources to elucidate the pathogen's epidemiology, evolution and antimicrobial resistance. We showed that ST34 has been introduced into Vietnam in at least nine occasions since 2000, forming five co-circulating major clones responsible for paediatric diarrhoea and bloodstream infection. Most expansion events were associated with acquisitions of large multidrug resistance plasmids of IncHI2 or IncA/C2. Particularly, the self-conjugative IncA/C2 pST34VN2 (co-transferring blaCTX-M-55, mcr-3.1, and qnrS1) underlies local expansion and intercontinental spread in two separate ST34 clones. At the global scale, Southeast Asia was identified as a potential hub for the emergence and dissemination of multidrug resistant Salmonella ST34, and mutation analysis suggests of selection in antimicrobial responses and key virulence factors.

© 2023. Springer Nature Limited.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1
Fig. 1. Global phylogeny ofSalmonella enterica ST34.
The figure displays the maximum likelihood phylogeny of 454 S. enterica ST34 isolates, constructed from 4962 single nucleotide polymorphisms (after removal of genomic regions pertaining to recombination). The phylogeny is rooted using anS. enterica ST19 outgroup. Branches are coloured in accordance to bootstrapping values, from low (cyan) to high (black). The rings present information associated with each taxon, in the following order (inner to outermost): (1) serotype predicted in silico from ST34 assemblies, (2) region of origin (for travel-associated isolates, the known travel destination was recorded as the region of origin), (3) population structure determined by hierarchical Bayesian clustering (BAPS), (4) source of isolation, and (5) disease manifestation (for isolates from Vietnam with clinical data). Colour shadings denote different clades (n ≥ 5 isolates) with clonal expansion in Vietnam, of which the majority of isolates originating from Vietnam or Southeast Asia. The horizontal bar indicates the number of substitution per site.
Fig. 2
Fig. 2. Temporal phylogenetic reconstruction ofSalmonella enterica ST34.
The panel (a) shows the maximum clade credibility (MCC) phylogeny of 222 representativeS. enterica ST34, constructed from 2671 single nucleotide polymorphisms (after removal of genomic regions pertaining to recombination). Branches are coloured according to the calculated posterior probability, from low (light blue) to high (black), while tip points are coloured based on the region of origin. The five clones associated with major clonal expansion events in Vietnam (VN1-4, VBSI) are annotated. The appended heatmap displays data associated with each taxon, including the predicted serotype (biphasic or monophasic Typhimurium), and the presence of antimicrobial resistance genes (blaCTX-M-55,qnrS1,mcr-3.1,mphA) and predominant plasmid replicon (IncA/C, IncHI2).b Estimation of the time to most common recent ancestor (tMRCA) of five major clonal expansions of ST34 (VN1-4, VBSI) in Vietnam, and (c) the distribution of acquired antimicrobial resistance genes in five major clonal expansions in Vietnam. For boxplots, bold central lines denote the median, the upper whisker extends from the 75th percentile to the highest value within the 1.5*interquartile range (IQR) of the hinge, the lower whisker extends from the 25th percentile to the lowest value within 1.5*IQR of the hinge. Data points beyond the end of the whiskers are outliers. Source data are provided in Supplementary Data 2.
Fig. 3
Fig. 3. Distribution of antimicrobial resistance (AMR) genes and plasmid types amongSalmonella enterica ST34 lineages.
For each panel, the bar graph displays the percentage of isolates from each lineage (BAPS-1 to -4) carrying a respective element, stratified by (a) genes conferring resistance to aminoglycosides, rifamycin (arr3), chloramphenicol, ampicillin (blaTEM), sulfonamides (sul2), tetracycline (tetB), (b) genes conferring resistance to macrolides, quinolone, colistin, and 3rd generation cephalosporins, and (c) plasmid incompatibility types. Source data are provided in Supplementary Data 2.
Fig. 4
Fig. 4. Phylogenetic structures ofSalmonella enterica ST34 clones carryingblaCTX-M-55.
Each panel displays a rooted phylogeny of a multidrug resistant clone, including (a) VN2, (b) Australia lineage 1 (Aus_L1), (c) Southeast Asia minor clone (SEA_min) and (d) China. Each phylogeny’s branches are coloured in accordance to bootstrapping values, from low (cyan) to high (black) (see legend). New included genomes, aside from those shown in Fig. 1, are marked with filled black circles on tips. The appended heatmap displays data associated with each taxon, including original country of isolation, host of isolation, presence of plasmid replicons (IncA/C2, IncHI2 and IncFII), IncFII-tra region incorporated on IncA/C2 plasmid, and resistance to critically important antimicrobials (blaCTX-M-55,mcr-3.1,qnrS1).
Fig. 5
Fig. 5. Phylogeography analysis ofSalmonella enterica ST34.
The figures display the results inferred from stochastic mapping (a) Circos plot denoting the transitions between the geographies (America, East Asia, Europe, Oceania, Southeast Asia). The broken outer ring represents the geographical sources of these transitions, proportional to their contributions to the total number of inferred transitions. Each block represents a transition direction between geographical states, with size proportional to the mean number of inferred transition events and colour based on the source of the transition.b The proportion of time spent in each geographical state. For both panels, the results are summarised from stochastic mapping runs of 1000 subsamplings of the maximum likelihood phylogeny described in Fig. 1. For boxplots, central lines denote the median, the upper whisker extends from the 75th percentile to the highest value within the 1.5*interquartile range (IQR) of the hinge, the lower whisker extends from the 25th percentile to the lowest value within 1.5*IQR of the hinge. Data points beyond the end of the whiskers are outliers. Source data are provided in Supplementary Data 2.
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