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A collection of 177 genomes of  Salmonella  Typhimurium and its monophasic variant isolated in 2014–2019 from Italian poultry/livestock ( n  = 165) and foodstuff ( n  = 12), previously screened for antimicrobial susceptibility and assigned to ST34 and single-locus variants, were studied in-depth to check the presence of the novel  mcr-9  gene and to investigate their genetic relatedness by whole genome sequencing (WGS). The study of accessory resistance genes revealed the presence of  mcr -9.1 in 11 ST34 isolates, displaying elevated colistin minimum inhibitory concentration values up to 2 mg/L and also a multidrug-resistant (MDR) profile toward up to seven antimicrobial classes. Five of them were also extended-spectrum beta-lactamases producers ( bla   SHV   –  12  type), mediated by the corresponding antimicrobial resistance (AMR) accessory genes. All  mcr -9-positive isolates harbored IncHI2-ST1 plasmids. From the results of the Mash analysis performed on all 177 genomes, the 11  mcr-9 -positive isolates fell together in the same subcluster and were all closely related. This subcluster included also two  mcr -9-negative isolates, and other eight  mcr -9-negative ST34 isolates were present within the same parental branch. All the 21 isolates within this branch presented an IncHI2/2A plasmid and a similar MDR gene pattern. In three representative  mcr -9-positive isolates,  mcr-9  was demonstrated to be located on different IncHI2/IncHI2A large-size (∼277–297 kb) plasmids, using a combined Illumina–Oxford Nanopore WGS approach. These plasmids were also compared by BLAST analysis with publicly available IncHI2 plasmid sequences harboring  mcr -9. In our plasmids,  mcr -9 was located in a ∼30-kb region lacking different genetic elements of the typical core structure of  mcr -9 cassettes. In this region were also identified different genes involved in heavy metal metabolism. Our results underline how genomics and WGS-based surveillance are increasingly indispensable to achieve better insights into the genetic environment and features of plasmid-mediated AMR, as in the case of such IncHI2 plasmids harboring other MDR genes beside  mcr -9, that can be transferred horizontally also to other major  Salmonella  serovars spreading along the food chain.

frontiers in microbiology

Emergence of IncHI2 Plasmids With Mobilized Colistin Resistance (mcr)-9 Gene in ESBL-Producing, Multidrug-Resistant Salmonella Typhimurium and Its Monophasic Variant ST34 From Food-Producing Animals in Italy