The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe.

Emeline Cherchame,Sangeeta Banerji,Federique Pasquali,Arnaud Felten,Eva Litrup,Liljana Petrovska,Pierre-Emmanuel Douarre,Pauline Barbet,Nana Mensah,Sabrina Cadel-Six,Sandra Simon,Michel-Yves Mistou,Michèle Gourmelon,Yue Tang,Maria Borowiak

doi:10.3389/fmicb.2021.651124

Abstract

The European epidemic monophasic variant of Salmonella enterica serovar Typhimurium (S. 1,4,[5],12:i:-) characterized by the multi locus sequence type ST34 and the antimicrobial resistance ASSuT profile has become one of the most common serovars in Europe (EU) and the United States (US). In this study, we reconstructed the time-scaled phylogeny and evolution of this Salmonella in Europe. The epidemic S. 1,4,[5],12:i:- ST34 emerged in the 1980s by an acquisition of the Salmonella Genomic Island (SGI)-4 at the 3′ end of the phenylalanine phe tRNA locus conferring resistance to copper and arsenic toxicity. Subsequent integration of the Tn21 transposon into the fljAB locus gave resistance to mercury toxicity and several classes of antibiotics used in food-producing animals (ASSuT profile). The second step of the evolution occurred in the 1990s, with the integration of mTmV and mTmV-like prophages carrying the perC and/or sopE genes involved in the ability to reduce nitrates in intestinal contents and facilitate the disruption of the junctions of the host intestinal epithelial cells. Heavy metals are largely used as food supplements or pesticide for cultivation of seeds intended for animal feed so the expansion of the epidemic S. 1,4,[5],12:i:- ST34 was strongly related to the multiple-heavy metal resistance acquired by transposons, integrative and conjugative elements and facilitated by the escape until 2011 from the regulatory actions applied in the control of S. Typhimurium in Europe. The genomic plasticity of the epidemic S. 1,4,[5],12:i:- was demonstrated in our study by the analysis of the plasmidome. We were able to identify plasmids harboring genes mediating resistance to phenicols, colistin, and fluoroquinolone and also describe for the first time in six of the analyzed genomes the presence of two plasmids (pERR1744967-1 and pERR2174855-2) previously described only in strains of enterotoxigenic Escherichia coli and E. fergusonii.

Highlights

The majority of the Salmonella serovars are motile; they can produce two types of flagellar proteins and switch from one type to the other by the expression regulation of fliC, fljBA, and hin genes
Typhimurium and 205 S. 1,4,[5],12:i:- ST34 human, animal, food, feed, and environmental isolates collected in Denmark, France, Germany, Italy, and the United Kingdom between 1992 and 2018
All identified Multi Locus Sequence Type (MLST) profiles in this study belong to the clade α described by Bawn et al (2020), with the exception of one strain (ERR2849932) that was assigned to ST313 and belonged to clade B

Summary

Introduction

The majority of the Salmonella serovars are motile; they can produce two types of flagellar proteins and switch from one type to the other by the expression regulation of fliC, fljBA, and hin genes. Since 2013, this serovar has become the third common cause of nontyphoidal Salmonella infections in Europe (European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC], 2014, 2015, 2016, 2017, 2018, 2019). 1,4,[5],12:i:- are commonly isolated in animal sources, they can be present in the environment such as surface waters. The major ST19 group revealed two high order clades (α and β) with clade α clustering the epidemic S. 1,4,[5],12:i:- ST34 (Bawn et al, 2020)

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