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

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

doi:10.3389/fmicb.2023.1304283

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

Front Microbiol. 2024 Jan 19:14:1304283. doi: 10.3389/fmicb.2023.1304283. eCollection 2023.

Authors

Jonah Feliza B Mora¹, Vanessa Yvonne B Meclat¹, Alyzza Marie B Calayag¹, Susana Campino², Julius C R Hafalla², Martin L Hibberd², Jody E Phelan², Taane G Clark^{2

3}, Windell L Rivera¹

Affiliations

¹ Pathogen-Host-Environment Interactions Research Laboratory, Institute of Biology, College of Science, University of the Philippines Diliman, Quezon City, Philippines.
² Department of Infection Biology, London School of Hygiene and Tropical Medicine, London, United Kingdom.
³ Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, United Kingdom.

Abstract

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.

Keywords: Salmonella enterica; antimicrobial resistance genes; food chains; plasmids; virulence; whole-genome sequencing.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The study was supported by the Department of Agriculture-Biotechnology Program Office, DABIOTECH-R1808: Using genomics to trace Salmonella transmission and antimicrobial resistance (AMR) in the poultry and swine food chains in Metropolitan Manila, Philippines and BBSRC UK-Philippines Swine & Poultry Research Initiative (BB/R013063/1). SC and TGC are supported by the Medical Research Council UK (Grant no. MR/M01360X/1, MR/N010469/1, MR/R020973/1, MR/X005895/1). The funders had no role in the study design, data collection, analysis, the decision to publish, or the preparation of the manuscript.