Long-term genomic surveillance reveals the circulation of clinically significant Salmonella in lymph nodes and beef trimmings from slaughter cattle from a Mexican feedlot

PLoS One. 2024 Oct 18;19(10):e0312275. doi: 10.1371/journal.pone.0312275. eCollection 2024.

Abstract

This longitudinal study characterized Salmonella circulating in lymph nodes (LN, n = 800) and beef trimmings (n = 745) from slaughter cattle from a Mexican feedlot. During two years, LN and beef trimming samples were collected 72-96 h post-slaughter, and we obtained 77 isolates of the serovars Anatum (n = 23), Reading (n = 22), Typhimurium (n = 10), London (n = 9), Kentucky (n = 6), Fresno (n = 4), Give, Muenster, and monophasic 1,4,[5],12:i- (n = 1 each). These isolates were subjected to whole genome sequencing, single-nucleotide polymorphism (SNP)-based phylogenetic analysis, reconstruction of their ancestral isolation sources through evolutionary analysis, and virulence profiling. Although LN and beef trimmings were not mixed, evolutionary analysis estimated that the common ancestor of all study isolates was likely of LN origin. Moreover, isolates from both sources were highly clonal (0-21 SNP distance), highlighting the complexity of Salmonella transmission dynamics. The pathogen persisted across cattle cohorts, as shown by clonality between isolates collected in different years (1-20 SNP distance). Major virulence genes were highly conserved (97-100% identity to the reference sequences) and most isolates carried a conserved version of pathogenicity islands 1-5, 9, 11, and 12. Typhimurium strains carried the Salmonella plasmid virulence operon (spvRABCD), and a Muenster isolate carried the st313td gene, both of which are associated with invasive phenotypes. Most isolates (49/77) were genetically similar (1-43 SNPs) to strains involved in human salmonellosis, highlighting their public health significance. Further research is needed on Salmonella transmission dynamics in cattle and the mechanisms determining subclinical infection and persistence in farm environments.

MeSH terms

  • Animals
  • Cattle
  • Cattle Diseases / microbiology
  • Longitudinal Studies
  • Lymph Nodes* / microbiology
  • Mexico
  • Phylogeny*
  • Polymorphism, Single Nucleotide*
  • Red Meat / microbiology
  • Salmonella / genetics
  • Salmonella / isolation & purification
  • Salmonella / pathogenicity
  • Salmonella Infections, Animal / microbiology
  • Virulence / genetics
  • Whole Genome Sequencing

Grants and funding

This research was funded by the National Autonomous University of Mexico (www.unam.mx), grant number PAPIIT IN212817, awarded to MSRL and OSR. Whole genome sequencing of isolates was conducted free of charge by the Mexican Department of Agriculture (Centro Nacional de Referencia de Inocuidad y Bioseguridad Agroalimentaria) (https://www.gob.mx/senasica/acciones-y-programas/servicios-del-centro-nacional-de-referencia-de-inocuidad-y-bioseguridad-de-inocuidad-y-bioseguridad-agroalimentaria). Mexico's National Council for Science and Technology (CONACYT) provided a fellowship for two MSc. students (AVGM and EAPH) that conducted their thesis dissertations within this project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.