Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes

The integration of next-generation sequencing into the identification and characterization of resistant and virulent strains as well as the routine surveillance of foodborne pathogens such as Salmonella enterica have not yet been accomplished in the Philippines. This study investigated the antimicro...

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Main Authors: Jonah Feliza B. Mora, Vanessa Yvonne B. Meclat, Alyzza Marie B. Calayag, Susana Campino, Julius C. R. Hafalla, Martin L. Hibberd, Jody E. Phelan, Taane G. Clark, Windell L. Rivera
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304283/full
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author Jonah Feliza B. Mora
Vanessa Yvonne B. Meclat
Alyzza Marie B. Calayag
Susana Campino
Julius C. R. Hafalla
Martin L. Hibberd
Jody E. Phelan
Taane G. Clark
Taane G. Clark
Windell L. Rivera
author_facet Jonah Feliza B. Mora
Vanessa Yvonne B. Meclat
Alyzza Marie B. Calayag
Susana Campino
Julius C. R. Hafalla
Martin L. Hibberd
Jody E. Phelan
Taane G. Clark
Taane G. Clark
Windell L. Rivera
author_sort Jonah Feliza B. Mora
collection DOAJ
description The integration of next-generation sequencing into the identification and characterization of resistant and virulent strains as well as the routine surveillance of foodborne pathogens such as Salmonella enterica have not yet been accomplished in the Philippines. This study investigated the antimicrobial profiles, virulence, and susceptibility of the 105 S. enterica isolates from swine and chicken samples obtained from slaughterhouses and public wet markets in Metropolitan Manila using whole-genome sequence analysis. Four predominant serovars were identified in genotypic serotyping, namely, Infantis (26.7%), Anatum (19.1%), Rissen (18.1%), and London (13.3%). Phenotypic antimicrobial resistance (AMR) profiling revealed that 65% of the isolates were resistant to at least one antibiotic, 37% were multidrug resistant (MDR), and 57% were extended-spectrum β-lactamase producers. Bioinformatic analysis revealed that isolates had resistance genes and plasmids belonging to the Col and Inc plasmid families that confer resistance against tetracycline (64%), sulfonamide (56%), and streptomycin (56%). Further analyses revealed the presence of 155 virulence genes, 42 of which were serovar-specific. The virulence genes primarily code for host immune system modulators, iron acquisition enzyme complexes, host cell invasion proteins, as well as proteins that allow intracellular and intramacrophage survival. This study showed that virulent MDR S. enterica and several phenotypic and genotypic AMR patterns were present in the food chain. It serves as a foundation to understand the current AMR status in the Philippines food chain and to prompt the creation of preventative measures and efficient treatments against foodborne pathogens.
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spelling doaj.art-22fed929b88843b987bf2d3508955f7e2024-01-19T11:09:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.13042831304283Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypesJonah Feliza B. Mora0Vanessa Yvonne B. Meclat1Alyzza Marie B. Calayag2Susana Campino3Julius C. R. Hafalla4Martin L. Hibberd5Jody E. Phelan6Taane G. Clark7Taane G. Clark8Windell L. Rivera9Pathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman, Quezon City, PhilippinesPathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman, Quezon City, PhilippinesPathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman, Quezon City, PhilippinesDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomDepartment of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, United KingdomPathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman, Quezon City, PhilippinesThe integration of next-generation sequencing into the identification and characterization of resistant and virulent strains as well as the routine surveillance of foodborne pathogens such as Salmonella enterica have not yet been accomplished in the Philippines. This study investigated the antimicrobial profiles, virulence, and susceptibility of the 105 S. enterica isolates from swine and chicken samples obtained from slaughterhouses and public wet markets in Metropolitan Manila using whole-genome sequence analysis. Four predominant serovars were identified in genotypic serotyping, namely, Infantis (26.7%), Anatum (19.1%), Rissen (18.1%), and London (13.3%). Phenotypic antimicrobial resistance (AMR) profiling revealed that 65% of the isolates were resistant to at least one antibiotic, 37% were multidrug resistant (MDR), and 57% were extended-spectrum β-lactamase producers. Bioinformatic analysis revealed that isolates had resistance genes and plasmids belonging to the Col and Inc plasmid families that confer resistance against tetracycline (64%), sulfonamide (56%), and streptomycin (56%). Further analyses revealed the presence of 155 virulence genes, 42 of which were serovar-specific. The virulence genes primarily code for host immune system modulators, iron acquisition enzyme complexes, host cell invasion proteins, as well as proteins that allow intracellular and intramacrophage survival. This study showed that virulent MDR S. enterica and several phenotypic and genotypic AMR patterns were present in the food chain. It serves as a foundation to understand the current AMR status in the Philippines food chain and to prompt the creation of preventative measures and efficient treatments against foodborne pathogens.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304283/fullSalmonella entericawhole-genome sequencingantimicrobial resistance genesplasmidsvirulencefood chains
spellingShingle Jonah Feliza B. Mora
Vanessa Yvonne B. Meclat
Alyzza Marie B. Calayag
Susana Campino
Julius C. R. Hafalla
Martin L. Hibberd
Jody E. Phelan
Taane G. Clark
Taane G. Clark
Windell L. Rivera
Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
Frontiers in Microbiology
Salmonella enterica
whole-genome sequencing
antimicrobial resistance genes
plasmids
virulence
food chains
title Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
title_full Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
title_fullStr Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
title_full_unstemmed Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
title_short Genomic analysis of Salmonella enterica from Metropolitan Manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
title_sort genomic analysis of salmonella enterica from metropolitan manila abattoirs and markets reveals insights into circulating virulence and antimicrobial resistance genotypes
topic Salmonella enterica
whole-genome sequencing
antimicrobial resistance genes
plasmids
virulence
food chains
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304283/full
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