Large-scale Genomic Survey of Non-typhoidal Salmonella enterica serovar Minnesota Strains in Chicken Products Reveals the Emergence of Multidrug Resistant Clones

Background: Salmonella enterica serovar Minnesota (S. Minnesota) is an emerging serovar of non-typhoidal Salmonella, known to persist in the food chain and distribution systems, potentially leading to outbreaks of Salmonella infections in human settings. Understanding the population genomics and dynamics of this pathogen is key to designing preventative measures and containing its spread within the poultry production chain. Methods: In this study, we conducted a large-scale study on S. Minnesota outbreak by fully characterizing population diversity and dynamics of a systematic collection from the poultry production chain in the Kingdom of Saudi Arabia (KSA). We sequenced 260 S. Minnesota strains from the western, eastern, and central regions of the country. We analyzed sequencing data to decipher the population diversity and dynamics of multidrug resistant strains and characterize the genetic basis of resistance and virulence. A hybrid long- and short-read sequencing approach was employed to analyze the population diversity of plasmids carrying antimicrobial resistance and virulence factors. Results: Our results indicate the rise of four clones (Bayesian Analysis of Population Structure; BAPS groups) in Saudi Arabia, three of which were mixed with global strains. The clones emerged over the past five to ten years and exhibited circulation between countries. The transmission analysis shows evidence of the spread of strains across cities, between countries, and mixing of strains from different suppliers, on epidemiological time scales. The emerging clones also harbored a higher resistance and virulence level than ancestral clones, owing to the acquisition of multiple plasmids, most importantly the IncC plasmid. The IncC plasmid was a mosaic plasmid, which carried antimicrobial resistance islands with blaCMY-2, ESBL blaCTX-M, aminoglycoside, and tetracycline resistance genes, as well as a hyperpathogenicity island with yersiniabactin genes. The plasmidome analysis revealed a high level of dynamics in the IncC plasmid structures with various configurations of resistance genes. Conclusion: Taken together, our results demonstrate a dynamic population and the emergence of multidrug-resistant clones in S. Minnesota. The results also highlight the role of plasmid acquisition and genomic variations in driving the concurrent evolution of pathogenicity and resistance in S. Minnesota.