Characterization and intestinal pathogenicity of Proteus mirabilis isolated from broiler carcasses and processing environments.

Abstract

Proteus mirabilis, a well-known urinary tract pathogen, is increasingly recognized as a food safety concern due to its frequent detection in meat products, particularly poultry. Sporadic reports indicate gastrointestinal symptoms linked to P. mirabilis, but the relationship between its genome, antibiotic resistance, and variable pathogenicity remains unclear. In this study, 142 P. mirabilis isolates were collected from broiler carcasses and processing environments in wet markets and industrial facilities to assess contamination levels. Thirty-six representative isolates were characterized for genomic heterogeneity, antibiotic resistance, and virulence gene profiles using whole-genome sequencing and phenotypic susceptibility testing. Selected strains were further assessed for intestinal pathogenicity in a murine model. Broiler carcasses from wet markets had significantly higher contamination rates (80.77 %, 21/26) than industrial sources (41.67 %, 5/12), with all wet market samples (13/13) testing positive. Overall, 94.4 % of isolates were multidrug-resistant, with carcass isolates showing higher resistance than environmental isolates. Animal experiments demonstrated variable pathogenicity, including intestinal injury, villus disruption, epithelial shedding, goblet cell loss, inflammatory cytokine elevation, and gut dysbiosis. Dysbiosis induced by certain strains (e.g., R638) was linked to intestinal injury, as confirmed by fecal microbiota transplantation. These findings highlight P. mirabilis as a highly heterogeneous foodborne pathogen, emphasizing the need for targeted hygiene practices, particularly in wet market processing environments.