Relationship and distribution of Salmonella enterica serovar I 4,[5],12:i:- strain sequences in the NCBI Pathogen Detection database

Authors: Trachsel, Julian; Bearson, Bradley - Brad; Brunelle, Brian; Bearson, Shawn

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/10/2022
Publication Date: 4/6/2022
Citation: Trachsel, J.M., Bearson, B.L., Brunelle, B.W., Bearson, S.M. 2022. Relationship and distribution of Salmonella enterica serovar I 4,[5],12:i:- strain sequences in the NCBI Pathogen Detection database. Biomed Central (BMC) Genomics. 23(1). Article 268. https://doi.org/10.1186/s12864-022-08458-z.
DOI: https://doi.org/10.1186/s12864-022-08458-z

Interpretive Summary: Salmonella is a common bacterial cause of human foodborne illness in the U.S. and globally. Salmonella subtypes are called serovars, and foodborne disease due to a serovar named I 4,[5],12:i:- has increased worldwide over the last two decades. Serovar I 4,[5],12:i:- is the most frequent multidrug-resistant (resistance to =3 antimicrobial types) Salmonella subtype detected in the U.S. Antimicrobials, such as antibiotics and in-feed metals, are used in food-animal production to control bacterial infections. Many Salmonella serovar I 4,[5],12:i:- strains contain a multidrug resistance module for resistance to four antibiotics and another genetic element called Salmonella Genomic Island 4 (SGI-4) with tolerance genes for metals, including copper which can be added to animal feed for pathogen control in food-animal production. We analyzed the genome sequences of 13,612 Salmonella serovar I 4,[5],12:i:- strains from a public database to determine the frequency of sequences containing antimicrobial resistance genes, the multidrug resistance module, SGI-4 with metal tolerance, and the frequency of animal-associated Salmonella sequences containing these attributes. Serovar I 4,[5],12:i:- strain sequences were available from 30 countries but sequences from the United States (59%) and the United Kingdom (28%) were the most common, likely because these countries contribute the most Salmonella genomes to the public database. The multidrug-resistance module and the metal tolerance island were present in 55% and 72% of serovar I 4,[5],12:i:- strain sequences, respectively. Swine-associated strain sequences of serovar I 4,[5],12:i:- were the most frequent food-animal source, and were significantly more likely to contain both multidrug-resistance genes and the metal tolerance island compared to other animal-associated isolate sequences. This investigation provides animal industry representatives as well as veterinary and medical community members with information on the presence of antimicrobial resistance, metal tolerance, and the animal sources associated with the bacterial foodborne pathogen Salmonella serovar I 4,[5],12:i:-.

Technical Abstract: Of the >2,600 Salmonella serovars, Salmonella enterica serovar I 4,[5],12:i:- (serovar I 4,[5],12:i:-) has emerged as one of the most common causes of human salmonellosis and the most frequent multidrug-resistant (MDR; resistance to =3 antimicrobial classes) nontyphoidal Salmonella serovar in the U.S. Serovar I 4,[5],12:i:- isolates have been described globally with resistance to ampicillin, streptomycin, sulfisoxazole, and tetracycline (R-type ASSuT) and a multi-metal tolerance island named Salmonella Genomic Island 4 (SGI-4). We analyzed 13,612 serovar I 4,[5],12:i:- strain sequences available in the NCBI Pathogen Detection database to determine global distribution, animal sources, presence of SGI-4, occurrence of R-type ASSuT, frequency of antimicrobial resistance (AMR), and potential transmission clusters. Genome sequences for serovar I 4,[5],12:i:- strains represented 30 countries from five continents (North America, Europe, Asia, Oceania, and South America), but sequences from the United States (59%) and the United Kingdom (28%) were dominant. The metal tolerance island SGI-4 and the R-type ASSuT were present in 72% and 55% of serovar I 4,[5],12:i:- strain sequences, respectively. Sixty-five percent of strain sequences were MDR which correlates to serovar I 4,[5],12:i:- being the most frequent MDR serovar. The distribution of serovar I 4,[5],12:i:- strain sequences in the NCBI Pathogen Detection database suggests that swine-associated strain sequences were the most frequent food-animal source and were significantly more likely to contain the metal tolerance island SGI-4 and genes for MDR compared to all other animal-associated isolate sequences.