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

Type Article
Date 2021-05
Language English
Author(s) Cadel-Six Sabrina1, Cherchame Emeline1, Douarre Pierre-Emmanuel1, Tang Yue2, Felten Arnaud1, Barbet Pauline1, Litrup Eva3, Banerji Sangeeta4, Simon Sandra4, Pasquali Federique5, Gourmelon MicheleORCID6, Mensah Nana2, Borowiak Maria7, Mistou Michel-Yves8, Petrovska Liljana2
Affiliation(s) 1 : Anses, Laboratory for Food Safety, Salmonella and Listeria Unit, Maisons-Alfort, France
2 : Department of Bacteriology, Animal and Plant Health Agency, Addlestone, United Kingdom
3 : Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark
4 : Robert Koch-Institute, Division of Enteropathogenic Bacteria and Legionella (FG11)/National Reference Centre for Salmonella and Other Bacterial Enteric Pathogens, Wernigerode, Germany
5 : Department of Agricultural and Food Sciences, Alma Mater Studiorum – University of Bologna, Bologna, Italy
6 : Ifremer, RBE, SGMM, Health, Environment and Microbiology Laboratory, Plouzané, France
7 : Department for Biological Safety, German Federal Institute for Risk Assessment (BfR), Berlin, Germany
8 : Université Paris-Saclay, INRAE, Centre International de Ressource Microbienne (CIRM) MaIAGE, Jouy-en-Josas, France
Source Frontiers In Microbiology (1664-302X) (Frontiers Media SA), 2021-05 , Vol. 12 , P. 651124 (16p.)
DOI 10.3389/fmicb.2021.651124
WOS© Times Cited 1
Keyword(s) epidemic monophasic Typhimurium, core and accessory genome phylogenetic analyses, Bayesian analysis, plasmidome, resistome, microevolution European study
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.

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Cadel-Six Sabrina, Cherchame Emeline, Douarre Pierre-Emmanuel, Tang Yue, Felten Arnaud, Barbet Pauline, Litrup Eva, Banerji Sangeeta, Simon Sandra, Pasquali Federique, Gourmelon Michele, Mensah Nana, Borowiak Maria, Mistou Michel-Yves, Petrovska Liljana (2021). The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe. Frontiers In Microbiology, 12, 651124 (16p.). Publisher's official version : https://doi.org/10.3389/fmicb.2021.651124 , Open Access version : https://archimer.ifremer.fr/doc/00696/80854/