Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters

ABSTRACT Surface waters function as ecological niches where Salmonella enterica can persist and disseminate to fresh produce production systems. We examined the genomic characteristics of S. enterica serotypes Agona (n = 86), Braenderup (n = 47), Muenchen (n = 53), and Panama (n = 69) isolates from...

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Main Authors: Zhao Chen, Enrique J. Delgado Suárez, Raquel R. Bonelli, Celso J. B. Oliveira, Andrea I. Moreno-Switt, Aiko D. Adell, Angélica Reyes-Jara, Christopher J. Grim, Marc W. Allard, Sandra M. Tallent, Eric W. Brown, Rebecca L. Bell, Magaly Toro, Jianghong Meng
Format: Article
Language:English
Published: American Society for Microbiology 2025-02-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.01706-24
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author Zhao Chen
Enrique J. Delgado Suárez
Raquel R. Bonelli
Celso J. B. Oliveira
Andrea I. Moreno-Switt
Aiko D. Adell
Angélica Reyes-Jara
Christopher J. Grim
Marc W. Allard
Sandra M. Tallent
Eric W. Brown
Rebecca L. Bell
Magaly Toro
Jianghong Meng
author_facet Zhao Chen
Enrique J. Delgado Suárez
Raquel R. Bonelli
Celso J. B. Oliveira
Andrea I. Moreno-Switt
Aiko D. Adell
Angélica Reyes-Jara
Christopher J. Grim
Marc W. Allard
Sandra M. Tallent
Eric W. Brown
Rebecca L. Bell
Magaly Toro
Jianghong Meng
author_sort Zhao Chen
collection DOAJ
description ABSTRACT Surface waters function as ecological niches where Salmonella enterica can persist and disseminate to fresh produce production systems. We examined the genomic characteristics of S. enterica serotypes Agona (n = 86), Braenderup (n = 47), Muenchen (n = 53), and Panama (n = 69) isolates from surface waters in Chile, Mexico, and Brazil between 2019 and 2022. Mexican isolates consistently displayed a higher occurrence of genotypic antimicrobial resistance (AMR) than Chilean and Brazilian isolates. All S. Agona isolates exhibited the presence of fosA7.2, while qnrB19 emerged as the predominant AMR gene (ARG) among S. Braenderup isolates. S. Muenchen isolates from Chile displayed an absence of any ARGs, while those from Mexico and Brazil predominantly carried qnrB19. Among S. Panama isolates from Chile, aadA1, floR, sat2, and tet(B) were the most prevalent ARGs, whereas those from Mexico and Brazil harbored tet(A), and floR and tet(A) as the leading ARGs, respectively. ARG sharing among isolates and ARG co-occurrence within individual isolates were prevalent across countries and serotypes. All isolates containing integrons exhibited genotypic multidrug resistance. The principal coordinates analysis reveals distinct clustering patterns based on country, serotype, number of ARGs per isolate, and plasmid and integron presence/absence. The whole-genome phylogenetic analysis demonstrates clear clusters, each associated with their respective countries. However, a notable exception was observed with one S. Agona isolate from Brazil closely related to two isolates from Chile, differing by only 18 and 19 single-nucleotide polymorphisms, respectively.IMPORTANCEThis comprehensive study explored the intricate genomic landscapes of S. Agona, Braenderup, Muenchen, and Panama isolates from surface waters across Chile, Mexico, and Brazil. By filling important knowledge gaps related to the genomic characteristics of these serotypes, the research offers a nuanced understanding of these serotypes as potential reservoirs for multidrug resistance. Our findings emphasize the urgency of targeted interventions to mitigate the emergence and dissemination of multidrug-resistant Salmonella enterica. This work underscores the need for informed policies and collaborative efforts to address the risks posed by S. enterica in Latin American surface waters.
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spelling doaj-art-525bdc32eafc461580f70cc0efb9ae3e2025-02-04T14:03:41ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-02-0113210.1128/spectrum.01706-24Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface watersZhao Chen0Enrique J. Delgado Suárez1Raquel R. Bonelli2Celso J. B. Oliveira3Andrea I. Moreno-Switt4Aiko D. Adell5Angélica Reyes-Jara6Christopher J. Grim7Marc W. Allard8Sandra M. Tallent9Eric W. Brown10Rebecca L. Bell11Magaly Toro12Jianghong Meng13Joint Institute for Food Safety and Applied Nutrition and Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, USAFacultad de Medicina Veterinaria y Zootecnia, Universidad de Nacional Autónoma de México, Mexico City, MexicoInstituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilDepartamento de Zootecnia, Universidade Federal da Paraíba, Areia, BrazilEscuela de Medicina Veterinaria, Facultad de Agronomía y Sistemas Naturales, Facultad de Ciencias Biológicas y Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, ChileEscuela de Medicina Veterinaria, Facultad de Ciencias de la Vida, Universidad Andrés Bello, Santiago, ChileInstituto de Nutrición y Tecnología de los Alimentos, Universidad de Chile, Santiago, ChileCenter for Food Safety and Applied Nutrition, USA Food and Drug Administration, College Park, Maryland, USACenter for Food Safety and Applied Nutrition, USA Food and Drug Administration, College Park, Maryland, USACenter for Food Safety and Applied Nutrition, USA Food and Drug Administration, College Park, Maryland, USACenter for Food Safety and Applied Nutrition, USA Food and Drug Administration, College Park, Maryland, USACenter for Food Safety and Applied Nutrition, USA Food and Drug Administration, College Park, Maryland, USAJoint Institute for Food Safety and Applied Nutrition and Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, USAJoint Institute for Food Safety and Applied Nutrition and Center for Food Safety and Security Systems, University of Maryland, College Park, Maryland, USAABSTRACT Surface waters function as ecological niches where Salmonella enterica can persist and disseminate to fresh produce production systems. We examined the genomic characteristics of S. enterica serotypes Agona (n = 86), Braenderup (n = 47), Muenchen (n = 53), and Panama (n = 69) isolates from surface waters in Chile, Mexico, and Brazil between 2019 and 2022. Mexican isolates consistently displayed a higher occurrence of genotypic antimicrobial resistance (AMR) than Chilean and Brazilian isolates. All S. Agona isolates exhibited the presence of fosA7.2, while qnrB19 emerged as the predominant AMR gene (ARG) among S. Braenderup isolates. S. Muenchen isolates from Chile displayed an absence of any ARGs, while those from Mexico and Brazil predominantly carried qnrB19. Among S. Panama isolates from Chile, aadA1, floR, sat2, and tet(B) were the most prevalent ARGs, whereas those from Mexico and Brazil harbored tet(A), and floR and tet(A) as the leading ARGs, respectively. ARG sharing among isolates and ARG co-occurrence within individual isolates were prevalent across countries and serotypes. All isolates containing integrons exhibited genotypic multidrug resistance. The principal coordinates analysis reveals distinct clustering patterns based on country, serotype, number of ARGs per isolate, and plasmid and integron presence/absence. The whole-genome phylogenetic analysis demonstrates clear clusters, each associated with their respective countries. However, a notable exception was observed with one S. Agona isolate from Brazil closely related to two isolates from Chile, differing by only 18 and 19 single-nucleotide polymorphisms, respectively.IMPORTANCEThis comprehensive study explored the intricate genomic landscapes of S. Agona, Braenderup, Muenchen, and Panama isolates from surface waters across Chile, Mexico, and Brazil. By filling important knowledge gaps related to the genomic characteristics of these serotypes, the research offers a nuanced understanding of these serotypes as potential reservoirs for multidrug resistance. Our findings emphasize the urgency of targeted interventions to mitigate the emergence and dissemination of multidrug-resistant Salmonella enterica. This work underscores the need for informed policies and collaborative efforts to address the risks posed by S. enterica in Latin American surface waters.https://journals.asm.org/doi/10.1128/spectrum.01706-24surface waterSalmonella entericawhole-genome sequencingantimicrobial resistancemultidrug resistanceintegron
spellingShingle Zhao Chen
Enrique J. Delgado Suárez
Raquel R. Bonelli
Celso J. B. Oliveira
Andrea I. Moreno-Switt
Aiko D. Adell
Angélica Reyes-Jara
Christopher J. Grim
Marc W. Allard
Sandra M. Tallent
Eric W. Brown
Rebecca L. Bell
Magaly Toro
Jianghong Meng
Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
Microbiology Spectrum
surface water
Salmonella enterica
whole-genome sequencing
antimicrobial resistance
multidrug resistance
integron
title Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
title_full Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
title_fullStr Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
title_full_unstemmed Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
title_short Exploring the genomic and antimicrobial resistance tapestry: comparative insights into Salmonella enterica serotypes Agona, Braenderup, Muenchen, and Panama in Latin American surface waters
title_sort exploring the genomic and antimicrobial resistance tapestry comparative insights into salmonella enterica serotypes agona braenderup muenchen and panama in latin american surface waters
topic surface water
Salmonella enterica
whole-genome sequencing
antimicrobial resistance
multidrug resistance
integron
url https://journals.asm.org/doi/10.1128/spectrum.01706-24
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