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The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe
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 stu...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8175864/ https://www.ncbi.nlm.nih.gov/pubmed/34093465 http://dx.doi.org/10.3389/fmicb.2021.651124 |
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author | Cadel-Six, Sabrina Cherchame, Emeline Douarre, Pierre-Emmanuel Tang, Yue Felten, Arnaud Barbet, Pauline Litrup, Eva Banerji, Sangeeta Simon, Sandra Pasquali, Federique Gourmelon, Michèle Mensah, Nana Borowiak, Maria Mistou, Michel-Yves Petrovska, Liljana |
author_facet | Cadel-Six, Sabrina Cherchame, Emeline Douarre, Pierre-Emmanuel Tang, Yue Felten, Arnaud Barbet, Pauline Litrup, Eva Banerji, Sangeeta Simon, Sandra Pasquali, Federique Gourmelon, Michèle Mensah, Nana Borowiak, Maria Mistou, Michel-Yves Petrovska, Liljana |
author_sort | Cadel-Six, Sabrina |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-8175864 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-81758642021-06-05 The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe Cadel-Six, Sabrina Cherchame, Emeline Douarre, Pierre-Emmanuel Tang, Yue Felten, Arnaud Barbet, Pauline Litrup, Eva Banerji, Sangeeta Simon, Sandra Pasquali, Federique Gourmelon, Michèle Mensah, Nana Borowiak, Maria Mistou, Michel-Yves Petrovska, Liljana Front Microbiol Microbiology 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. Frontiers Media S.A. 2021-05-21 /pmc/articles/PMC8175864/ /pubmed/34093465 http://dx.doi.org/10.3389/fmicb.2021.651124 Text en Copyright © 2021 Cadel-Six, Cherchame, Douarre, Tang, Felten, Barbet, Litrup, Banerji, Simon, Pasquali, Gourmelon, Mensah, Borowiak, Mistou and Petrovska. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Cadel-Six, Sabrina Cherchame, Emeline Douarre, Pierre-Emmanuel Tang, Yue Felten, Arnaud Barbet, Pauline Litrup, Eva Banerji, Sangeeta Simon, Sandra Pasquali, Federique Gourmelon, Michèle Mensah, Nana Borowiak, Maria Mistou, Michel-Yves Petrovska, Liljana The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title | The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title_full | The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title_fullStr | The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title_full_unstemmed | The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title_short | The Spatiotemporal Dynamics and Microevolution Events That Favored the Success of the Highly Clonal Multidrug-Resistant Monophasic Salmonella Typhimurium Circulating in Europe |
title_sort | spatiotemporal dynamics and microevolution events that favored the success of the highly clonal multidrug-resistant monophasic salmonella typhimurium circulating in europe |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8175864/ https://www.ncbi.nlm.nih.gov/pubmed/34093465 http://dx.doi.org/10.3389/fmicb.2021.651124 |
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