Genomic Analysis of Salmonella enterica Serovar Typhimurium from Wild Passerines in England and Wales.

UNLABELLED: Passerine salmonellosis is a well-recognized disease of birds in the order Passeriformes, which includes common songbirds such as finches and sparrows, caused by infection with Salmonella enterica serovar Typhimurium. Previous research has suggested that some subtypes of S Typhimurium-definitive phage types (DTs) 40, 56 variant, and 160-are host adapted to passerines and that these birds may represent a reservoir of infection for humans and other animals. Here, we have used the whole-genome sequences of 11 isolates from British passerines, five isolates of similar DTs from humans and a domestic cat, and previously published S Typhimurium genomes that include similar DTs from other hosts to investigate the phylogenetic relatedness of passerine salmonellae to other S Typhimurium isolates and investigate possible genetic features of the distinct disease pathogenesis of S Typhimurium in passerines. Our results demonstrate that the 11 passerine isolates and 13 other isolates, including those from nonpasserine hosts, were genetically closely related, with a median pairwise single nucleotide polymorphism (SNP) difference of 130 SNPs. These 24 isolates did not carry antimicrobial resistance genetic determinants or the S Typhimurium virulence plasmid. Although our study does not provide evidence of Salmonella transmission from passerines to other hosts, our results are consistent with the hypothesis that wild birds represent a potential reservoir of these Salmonella subtypes, and thus, sensible personal hygiene precautions should be taken when feeding or handling garden birds. IMPORTANCE: Passerine salmonellosis, caused by certain definitive phage types (DTs) of Salmonella Typhimurium, has been documented as a cause of wild passerine mortality since the 1950s in many countries, often in the vicinity of garden bird feeding stations. To gain better insight into its epidemiology and host-pathogen interactions, we sequenced the genomes of a collection of 11 isolates from wild passerine salmonellosis in England and Wales. Phylogenetic analysis showed these passerine isolates to be closely related to each other and to form a clade that is distinct from other strains of S Typhimurium, which included a multidrug-resistant isolate from invasive nontyphoidal Salmonella disease that shares the same phage type as several of the passerine isolates. Closely related to wild passerine isolates and within the same clade were four S Typhimurium isolates from humans as well as isolates from horses, poultry, cattle, an unspecified wild bird, and a domestic cat and dog with similar DTs and/or multilocus sequence types. This suggests the potential for cross-species transmission, and the genome sequences provide a valuable resource to investigate passerine salmonellosis further.

AEM was supported by Wellcome Trust grant 098051 whilst at the Wellcome Trust Sanger Institute, and a Biotechnology and Biological Sciences Research Council grant BB/M014088/1 at the University of Cambridge. GKP and sequencing were supported by a Medical Research Council Partnership Grant (G1001787/1) held by MAH at the Department of Veterinary Medicine, University of Cambridge. The Garden Bird Health initiative received financial support from the British Veterinary Association Animal Welfare Foundation, CJ Wildbird Foods Ltd., Cranswick Pet Products, Defra (through the Animal & Plant Health Agency’s Diseases of Wildlife Scheme), Birdcare Standards Association and the Universities Federation for Animal Welfare. JP, NRT, AJP, and the sequencing were also supported by the Wellcome Trust, grant number 098051. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

This is the author accepted manuscript. The final version is available from the American Society for Microbiology via https://doi.org/10.1128/aem.01660-16