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

Abstract

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.

The challenging task to select Salmonella target serovars in poultry: the Italian point of view

“…However, the data presented here confirm that this serovar does indeed occur in breeding birds at the top of the poultry production pyramid. Another important factor deserving particular attention is that S. Napoli has been associated with typhoidal serovars thanks to their genetic similarities, and hence, its control along the food chain is of paramount importance [10].…”

“…Another important factor deserving particular attention is that S . Napoli has been associated with typhoidal serovars thanks to their genetic similarities, and hence, its control along the food chain is of paramount importance [ 10 ].…”

Global Spread and Molecular Characterization of CTX-M-Producing Salmonella Typhimurium Isolates

“…According to the WHO, there over 90 million people are infected by Salmonella annually, and 150,000 people die from Salmonella infection [ 1 ]. Over 2600 Salmonella serotypes have been identified and can be referred to as typhoidal or non-typhoidal (NTS); the latter are present in different animal reservoirs and are responsible for self-limiting gastrointestinal syndromes [ 2 ]. S. Typhimurium can cause potential threat to human health through the consumption of contaminated food or water [ 3 ].…”

Effect of pH and Salinity on the Ability of Salmonella Serotypes to Form Biofilm

“…Based on epidemiological evidences collected in Italy, Leati et al (2021) suggested that other serotypes, such as Salmonella Derby and Salmonella Napoli, should be considered for control at primary production level, due to their frequent isolation in human infections. In addition, it has increasingly been reported that specific clones of different serotypes, rather than the serotype as such, are responsible for emergent spread in both humans and the food chain ( Coipan et al, 2020 ; García-Soto et al, 2020 ; Mastrorilli et al, 2020 ; EFSA and ECDC, 2021b ). Often, these clones are characterized by the acquisition of large conjugative plasmids providing resistance features and virulence-associated properties ( Franco et al, 2015 ; Alba et al, 2020 ; García-Soto et al, 2020 ).…”