Large-scale Genomic Survey of Non-typhoidalSalmonella entericaserovar Minnesota Strains in Chicken Products Reveals the Emergence of Multidrug Resistant Clones

Author:

Huang Jiayi,Alzahrani Khaloud O.,Zhou Ge,Alsalman Shahad A.,Almansour Ayidh M.,Alhadlaq Meshari A.,Alhussain Shaykhah,Alajlan Abdullah A.,Al-Akeel Saleh I.,Al Rashidy Malfi S.,Alzauhair Abdulrahman,AlReshoodi Fahad M.,Alsufyani Amani T.,Alotaibi Nourah M.,Althubaiti Afnan,Alshdokhi Elaf,Alhamed Ashwaq,Almusa Manal,Almadi Talah,Almutairi Nouf,Mukhtar Lenah E.,AlHarbi Abdulmohsen L.,Banzhaf Manuel,Milner Mathew,AlArawi Mohammad,Alajel Sulaiman,Moradigaravand Danesh

Abstract

AbstractBackgroundSalmonella entericaserovar Minnesota (S. Minnesota) is an emerging serovar of non-typhoidalSalmonella, known to persist in the food chain and distribution systems, potentially leading to outbreaks ofSalmonellainfections 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.MethodsIn this study, we conducted a large-scale study onS. 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 260S. 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.ResultsOur 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 withblaCMY-2, ESBLblaCTX-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.ConclusionTaken together, our results demonstrate a dynamic population and the emergence of multidrug-resistant clones inS. Minnesota. The results also highlight the role of plasmid acquisition and genomic variations in driving the concurrent evolution of pathogenicity and resistance inS. Minnesota.

Publisher

Cold Spring Harbor Laboratory

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