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Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017

BACKGROUND: Salmonella enterica subsp. enterica serovar Napoli (S. Napoli) is among the top serovars causing human infections in Italy, although it is relatively uncommon in other European countries; it is mainly isolated from humans and the environment, but neither the reservoir nor its route of in...

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Autores principales: Mastrorilli, Eleonora, Petrin, Sara, Orsini, Massimiliano, Longo, Alessandra, Cozza, Debora, Luzzi, Ida, Ricci, Antonia, Barco, Lisa, Losasso, Carmen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7057659/
https://www.ncbi.nlm.nih.gov/pubmed/32131727
http://dx.doi.org/10.1186/s12864-020-6588-y
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author Mastrorilli, Eleonora
Petrin, Sara
Orsini, Massimiliano
Longo, Alessandra
Cozza, Debora
Luzzi, Ida
Ricci, Antonia
Barco, Lisa
Losasso, Carmen
author_facet Mastrorilli, Eleonora
Petrin, Sara
Orsini, Massimiliano
Longo, Alessandra
Cozza, Debora
Luzzi, Ida
Ricci, Antonia
Barco, Lisa
Losasso, Carmen
author_sort Mastrorilli, Eleonora
collection PubMed
description BACKGROUND: Salmonella enterica subsp. enterica serovar Napoli (S. Napoli) is among the top serovars causing human infections in Italy, although it is relatively uncommon in other European countries; it is mainly isolated from humans and the environment, but neither the reservoir nor its route of infection are clearly defined. This serovar is characterized by high genomic diversity, and molecular evidences revealed important similarities with typhoidal serovars. RESULTS: 179 S. Napoli genomes as well as 239 genomes of typhoidal and non-typhoidal serovars were analyzed in a comparative genomic study. Phylogenetic analysis and draft genome characterization in terms of Multi Locus Sequence Typing (MLST), plasmid replicons, Salmonella Pathogenicity Islands (SPIs), antimicrobial resistance genes (ARGs), phages, biocide and metal-tolerance genes confirm the high genetic variability of S. Napoli, also revealing a within-serovar phylogenetic structure more complex than previously known. Our work also confirms genomic similarity of S. Napoli to typhoidal serovars (S. Typhi and S. Paratyphi A), with S. Napoli samples clustering primarily according to ST, each being characterized by specific genomic traits. Moreover, two major subclades of S. Napoli can be clearly identified, with ST-474 being biphyletic. All STs span among isolation sources and years of isolation, highlighting the challenge this serovar poses to define its epidemiology and evolution. Altogether, S. Napoli strains carry less SPIs and less ARGs than other non-typhoidal serovars and seldom acquire plasmids. However, we here report the second case of an extended-spectrum β–lactamases (ESBLs) producing S. Napoli strain and the first cases of multidrug resistant (MDR) S. Napoli strains, all isolated from humans. CONCLUSIONS: Our results provide evidence of genomic plasticity of S. Napoli, highlighting genomic similarity with typhoidal serovars and genomic features typical of non-typhoidal serovars, supporting the possibility of survival in different niches, both enteric and non-enteric. Presence of horizontally acquired ARGs and MDR profiles rises concerns regarding possible selective pressure exerted by human environment on this pathogen.
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spelling pubmed-70576592020-03-10 Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017 Mastrorilli, Eleonora Petrin, Sara Orsini, Massimiliano Longo, Alessandra Cozza, Debora Luzzi, Ida Ricci, Antonia Barco, Lisa Losasso, Carmen BMC Genomics Research Article BACKGROUND: Salmonella enterica subsp. enterica serovar Napoli (S. Napoli) is among the top serovars causing human infections in Italy, although it is relatively uncommon in other European countries; it is mainly isolated from humans and the environment, but neither the reservoir nor its route of infection are clearly defined. This serovar is characterized by high genomic diversity, and molecular evidences revealed important similarities with typhoidal serovars. RESULTS: 179 S. Napoli genomes as well as 239 genomes of typhoidal and non-typhoidal serovars were analyzed in a comparative genomic study. Phylogenetic analysis and draft genome characterization in terms of Multi Locus Sequence Typing (MLST), plasmid replicons, Salmonella Pathogenicity Islands (SPIs), antimicrobial resistance genes (ARGs), phages, biocide and metal-tolerance genes confirm the high genetic variability of S. Napoli, also revealing a within-serovar phylogenetic structure more complex than previously known. Our work also confirms genomic similarity of S. Napoli to typhoidal serovars (S. Typhi and S. Paratyphi A), with S. Napoli samples clustering primarily according to ST, each being characterized by specific genomic traits. Moreover, two major subclades of S. Napoli can be clearly identified, with ST-474 being biphyletic. All STs span among isolation sources and years of isolation, highlighting the challenge this serovar poses to define its epidemiology and evolution. Altogether, S. Napoli strains carry less SPIs and less ARGs than other non-typhoidal serovars and seldom acquire plasmids. However, we here report the second case of an extended-spectrum β–lactamases (ESBLs) producing S. Napoli strain and the first cases of multidrug resistant (MDR) S. Napoli strains, all isolated from humans. CONCLUSIONS: Our results provide evidence of genomic plasticity of S. Napoli, highlighting genomic similarity with typhoidal serovars and genomic features typical of non-typhoidal serovars, supporting the possibility of survival in different niches, both enteric and non-enteric. Presence of horizontally acquired ARGs and MDR profiles rises concerns regarding possible selective pressure exerted by human environment on this pathogen. BioMed Central 2020-03-04 /pmc/articles/PMC7057659/ /pubmed/32131727 http://dx.doi.org/10.1186/s12864-020-6588-y Text en © The Author(s). 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Mastrorilli, Eleonora
Petrin, Sara
Orsini, Massimiliano
Longo, Alessandra
Cozza, Debora
Luzzi, Ida
Ricci, Antonia
Barco, Lisa
Losasso, Carmen
Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title_full Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title_fullStr Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title_full_unstemmed Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title_short Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017
title_sort comparative genomic analysis reveals high intra-serovar plasticity within salmonella napoli isolated in 2005–2017
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7057659/
https://www.ncbi.nlm.nih.gov/pubmed/32131727
http://dx.doi.org/10.1186/s12864-020-6588-y
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