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Salmonella enterica subsp. enterica serovar Gallinarum biovar pullorum (Salmonella pullorum) is an avian-specific pathogen that has caused considerable economic losses to the poultry industry. High endemicity, poor implementation of hygiene measures, and lack of effective vaccines hinder the prevention and control of this disease in intensively maintained poultry flocks. In recent years, the incidence of arthritis in chicks caused by Salmonella pullorum infection has increased. In this study, four Salmonella pullorum strains were identified from the livers, spleens, and joint fluids of Qingjiaoma chicken breeders with arthritis clinical signs, and an arthritis model of chicks was successfully established using SP206-2. Whole genome sequencing of the SP206-2 strain showed that the genome was 4,730,579 bp, 52.16% GC content, and contained 5007 genes, including 4729 protein-coding regions. The genomic analysis of four arthritis-causing isolates and three diarrhea-causing isolates showed that the genome of arthritis-causing isolates was subject to nonsynonymous mutations, shift mutations, and gene copy deletions. An SNP phylogenetic tree analysis showed that arthritis-causing isolates are located in a different evolutionary branch from diarrhea-causing isolates. Further differential genes analysis showed that the genome of arthritis-causing isolates had missense mutations in genes related to substance metabolism and substance transport, as a result of adaptive evolution.

Salmonella enterica is considered a significant threat to the global poultry industry and public health. In recent decades, antimicrobial resistance in Salmonella enterica has attracted increasing concern throughout the world. However, limited information is available on Salmonella enterica among different breeds of breeder chickens. Thus, this study aimed to compare the prevalence, serotype distribution, emergence of extended-spectrum beta-lactamases (ESBLs), antimicrobial resistance, and genetic resistance mechanisms in Salmonella enterica among different breeds of breeder chickens. A total of 693 samples (dead embryos, cloacal swabs, water, feed, environmental swabs, and meconium of newly hatched chicks) were selected and cultured for Salmonella from four breeder chicken farms in Shandong province, China, representing one imported and three native breeds, and the isolates were further serotyped. Of the Salmonella isolates, susceptibility to 11 antimicrobials of 5 classes, ESBL screening, and the presence of 21 antimicrobial resistance genes were determined in the present study. Overall, 94 (13.6%) isolates were recovered, which were divided into 3 serotypes (Salmonella Pullorum (n = 36), Salmonella Thompson (n = 32), and Salmonella Enteritidis (n = 26)). The results showed that the prevalence of Salmonella enterica isolates from the imported breeds was higher compared with the three domestic breeds. Eight of the ninety-four isolates were ESBL-positive strains, which were recovered from a domestic breed chicken farm. These eight ESBL-producing isolates were serotyped to Pullorum. Surprisingly, Salmonella Enteritidis (S. enteritidis) and S. pullorum were simultaneously isolated from a single dead embryo observed among one native breed. Meanwhile, among the Salmonella isolates, 53.2% (50/94) were multidrug-resistant strains, and 44.7% (42/94) of the isolates presented resistance to at least five antibiotics. Nearly all of the isolates (97.9%, 92/94) were resistant to at least one antimicrobial; one isolate of S. Thompson was resistant to seven antimicrobial agents belonging to four different classes. The carriage rate of three resistance genes (tetA, tetB, and sul1) among isolates from the imported breeds (87%, 70%, and 65.2%) was higher than that in those from domestic breeds (35.2%, 36.6, and 14.1%). To our knowledge, this is the first report of ESBLs-producing Salmonella isolated from a Chinese native breed of breeder chickens. Our results also highlight that a high prevalence of multidrug-resistant Salmonella enterica contamination is widespread among different breeds of breeder chickens, which is a major risk of food-borne diseases and public health.