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Moreno-Switt, A. I.

Publications and source records attributed to Moreno-Switt, A. I..

4 recordsLinked to original sources

Prophage {Phi}ESI promotes competitive dominance in the emergent Salmonella serovar Infantis lineage

The global spread of multidrug-resistant Salmonella enterica serovar Infantis has been largely attributed to the pESI megaplasmid, yet additional factors underlying the ecological success of this lineage remain unclear. Here, we characterize {Phi}ESI (phage of emergent Salmonella Infantis), a temperate bacteriophage discovered during coculture of an emergent pESI-positive strain (PM57) and a non-emergent strain (DR006). Phage {Phi}ESI shows a siphovirus morphotype with a long tail and an elongated head, with a genome of 46,490 bp, which is integrated as a prophage in the 3-end of an Arg-tRNA gene in PM57, but is absent in DR006, which is susceptible to the {Phi}ESI-mediated lysis. The screening of {Phi}ESI genes across 20,429 global Salmonella Infantis genomes revealed an almost exclusive association of {Phi}ESI and {Phi}ESI-like phages with the emergent pESI-positive Salmonella Infantis lineage. Further bioinformatic analyses of complete chromosomes revealed diverse {Phi}ESI insertion profiles showing geographic clustering, and the presence of large-scale chromosomal inversions flanked by {Phi}ESI genes. Competition assays showed that PM57 outcompeted DR006 in coculture, coinciding with high viral loads that selectively targeted DR006, and susceptibility assays showed that strains lacking {Phi}ESI/{Phi}ESI-like prophages were susceptible to {Phi}ESI-mediated lysis. Together, our findings identify {Phi}ESI as a competitive factor associated with emergent Salmonella Infantis, able to selectively eliminate susceptible competitors. Our findings suggest that {Phi}ESI/{Phi}ESI-like prophages contributed to the persistence and global dissemination of the emergent Salmonella Infantis lineage. ImportanceEmergent multidrug-resistant Salmonella enterica serovar Infantis strains carrying pESI megaplasmids have spread worldwide, posing a global public health threat and a significant economic burden. Nevertheless, the factors contributing to the success of this foodborne pathogen, beyond pESI, remain poorly understood. Here, we describe {Phi}ESI, a novel temperate bacteriophage carried by the emergent lineage as a chromosomally integrated prophage. We show that {Phi}ESI provides a competitive advantage to emergent strains by selectively killing non-emergent competitors while protecting lysogens from reinfection. Our findings uncover the contribution of {Phi}ESI/{Phi}ESI-like bacteriophages to the success of emergent Salmonella Infantis, highlighting how lineage-associated prophages can shape the ecological success of pathogenic bacteria.

microbiology↗

Emergence of a multidrug-resistant Salmonella enterica serovar Amager lineage carrying the blaCTX-M-65-positive pESI megaplasmid

The spread of extended-spectrum {beta}-lactamase (ESBL)-producing and fluoroquinolone-resistant Salmonella pose a global public health challenge in addition to the high burden of infections associated with this foodborne pathogen. In this study we aimed to characterize a multidrug-resistant strain of Salmonella serovar Amager isolated from a Chilean river in October 2023. Antimicrobial susceptibility testing revealed a resistance phenotype against multiple antibiotic families, including fluoroquinolones and {beta}-lactams, showing ESBL production. Hybrid genome sequencing allowed the identification of a 311,303 bp plasmid carrying the aadA1, aph(4)-Ia, aac(3)-IVa, floR, sul1, tet(A), and blaCTX-M-65 genes, sharing 99.98% sequence identity with the Salmonella Infantis pESI-like megaplasmid. In addition, the qnrB19 gene was found in a {approx}2.7 kbp plasmid of widespread distribution. Population structure and temporal phylogenetic analysis at the global scale revealed the emergence of a Salmonella Amager lineage from the HC20_35565 cluster, carrying the Salmonella Infantis blaCTX-M-65-positive pESI-like megaplasmid and causing human infections in the United States and the United Kingdom. Our work describes the emergence of a Salmonella lineage with resistance against first-line antibiotics used for treating severe infections, underscoring the relevance of environmental surveillance as a means for detecting emergent pathogens and anticipating human infections.

genomics↗

Emergent Salmonella enterica serovar Infantis forms a monophyletic lineage shaped by geographic structuring

Multidrug-resistant Salmonella Infantis carrying pESI-like megaplasmids have disseminated worldwide representing a serious threat to public health. Previous studies have investigated its population structure and temporal dynamics above the continental level. However, their conclusions were constrained by limited datasets and sampling biases. To address these issues, we analyzed all publicly available Salmonella Infantis genomes to characterize its global population structure and phylogeographic dispersal. We selected a non-redundant dataset of 14,012 genomes representing the temporal, geographic, isolation source, and genomic diversity of Salmonella Infantis from 78 countries across five continents, collected between 1910 to 2024. Phylogenomic analyses showed that emergent megaplasmid-positive Salmonella Infantis forms a monophyletic lineage with significant geographic structuring. The megaplasmid-positive lineage was inferred to be originated in West Asia around 1990, followed by multiple introductions into Europe and a single transmission to South America which resulted in the dissemination of this pathogen to Northern America, and from there to the rest of the continent. Multiple recent transmission events of the American lineage to all continents were observed, driving the dispersal of the blaCTX-M-65 gene encoding extended-spectrum {beta}-lactamases. Moreover, genomic evidence also suggests that the emergence of ESBL-producing strains in parts of Asia and Africa may be associated to poultry trading from the Americas. Our findings underscore the urgent need for integrating global human, animal, and environmental surveillance data with population genomic analyses to contain the threats posed by ESBL-producing Salmonella Infantis.

genomics↗

Widespread dissemination of ESBL-producing Salmonella enterica serovar Infantis exhibiting intermediate fluoroquinolone resistance and harboring blaCTX-M-65-positive pESI-like megaplasmids in Chile

BackgroundMultidrug-resistant (MDR) Salmonella Infantis has disseminated worldwide, mainly linked to the consumption of poultry products. Evidence shows dissemination of this pathogen in Chile; however, studies are primarily limited to phenotypic data or involve few isolates. As human cases of Salmonella Infantis infections have substantially increased in recent years, a better understanding of its molecular epidemiology and antimicrobial-resistance profiles are required to inform effective surveillance and control measures. MethodsWe sequenced 396 Salmonella Infantis genomes and analyzed them with all publicly available genomes of this pathogen from Chile (440 genomes in total), representing isolates from environmental, food, animal, and human sources obtained from 2009 to 2022. Based on bioinformatic and phenotypic methods, we assessed the population structure, dissemination among different niches, and AMR profiles of Salmonella Infantis in the country. FindingsThe genomic and phylogenetic analyses showed that Salmonella Infantis from Chile comprised several clusters of highly related isolates dominated by sequence type 32. The HC20_343 cluster grouped an important proportion of all isolates. The latter was the only cluster associated with pESI-like megaplasmids, and up to 12 acquired AMR genes/mutations predicted to result in an MDR phenotype. Accordingly, antimicrobial-susceptibility testing revealed a strong concordance between the AMR genetic determinants and their matching phenotypic expression, indicating that a significant proportion of HC20_343 isolates produce extended- spectrum {beta}-lactamases and have intermediate fluoroquinolone resistance. HC20_343 Salmonella Infantis were spread among environmental, animal, food, and human niches, showing a close relationship between isolates from different years and sources, and a low intra-source genomic diversity. InterpretationOur findings show a widespread dissemination of MDR Salmonella Infantis from the HC20_343 cluster in Chile. The high proportion of isolates with resistance to first-line antibiotics and the evidence of active transmission between the environment, animals, food, and humans highlight the urgency of improved surveillance and control measures in the country. As HC20_343 isolates predominate in the Americas, our results suggest a high prevalence of ESBL- producing Salmonella Infantis with intermediate fluoroquinolone resistance in the continent. FundingAgencia de Investigacion y Desarrollo de Chile (ANID) through FONDECYT de Postdoctorado Folio 3230796 and Folio 3210317, FONDECYT Regular Folio 1231082, and ANID - Millennium Science Initiative Program - ICN2021_044. Research in contextO_ST_ABSEvidence before the studyC_ST_ABSIn the last decade, emergent multidrug-resistant Salmonella Infantis has spread worldwide, primarily linked to poultry product consumption. However, in most countries from the Americas Region, such as Chile, the extent of the dissemination of emergent Salmonella Infantis and its molecular epidemiology remains unknown. In May and September 2023, an online search was conducted using the Google engine and the PMC database with the terms "Salmonella," "Infantis," and "Chile," with no language restrictions. We assessed the results to select those presenting antimicrobial resistance, epidemiologic, or genomic data directly associated with isolates from Chile (13 studies). The selected studies showed that the prevalence of Salmonella Infantis in poultry-meat production systems, its resistance to different antibiotics, and the number of human cases of infection caused by this serovar have increased since 2014-2016. However, these reports were limited to phenotypic data or involved the genomic analysis of a few isolates (<50) obtained from the same source. No study has assessed the genomic epidemiology of the Salmonella Infantis population at the country level. Added value of this studyHere, we present the first large-scale genomic epidemiology analysis of Salmonella Infantis in Chile, including isolates from environmental, food, animal, and human sources obtained from 2009 to 2022. We found that Salmonella Infantis in Chile is divided into several clusters of highly related isolates and that only a single cluster, the HC20_343, was associated with multiple antimicrobial-resistance determinants and pESI-like megaplasmids. We also report that isolates from this cluster are widespread among most sources, including irrigation water, poultry, food, and human cases. Detection of AMR determinants coupled with antimicrobial- susceptibility testing indicated that most HC20_343 isolates are ESBL-producers and have intermediate resistance to ciprofloxacin. Population structure analysis of this foodborne pathogen evidenced an active transmission of MDR Salmonella Infantis between different niches. This study reveals the widespread dissemination of MDR Salmonella Infantis in Chile. Implications of all the available evidenceThe evidence indicates that emerging Salmonella Infantis from the HC20_343 cluster is spreading among various niches, including irrigation water, poultry, and food, causing human infections in Chile. Its resistance to first-line antibiotics used for treating salmonellosis in individuals with a higher risk of severe or invasive infections is concerning. Currently, most surveillance and control efforts to reduce salmonellosis in Chile are focused on the poultry industry, and the study of outbreaks does not include whole-genome sequence analyses. Our findings highlight the urgent necessity to improve the surveillance and control measures to include agricultural waters to prevent contamination of produce and the further dissemination of resistance genes in the environment. As the HC20_343 cluster is highly prevalent in the Americas, further research involving large-scale genomic population analyses would shed light on the extent of the dissemination and transmission routes of emergent Salmonella Infantis in the continent and may contribute to informing surveillance and control policies.

genomics↗