Genomic analysis of multidrug-resistant Salmonellaenterica Serovar Montevideo isolates in China

As an important foodborne bacterium, non-typhoidal Salmonella (NTS) is estimated to cause approximately 215,000 deaths worldwide each year. Globally, S. Montevideo has been reported to cause several outbreaks, with low frequencies of antimicrobial resistance (AMR). In China, the information on S. Montevideo isolates was limited, especially the genomic data. This study aimed to characterize the phenotypic and genomic features of 26 S. Montevideo isolates collected in China between 2018 and 2024. During this period, 26 S. Montevideo isolates were collected from different sources in five provinces or municipalities in China. Minimum inhibitory concentrations (MICs) of nine antimicrobial agents were determined using the broth microdilution method. Isolates were sequenced on the Illumina platform to identify antimicrobial resistance genes, virulence genes, mobile genetic elements (MGEs), and phylogenetic relationships with global isolates.

The whole length of the 26 assembled genome sequences ranged from 4,612,761 bp to 5,071,299 bp. There were three sequence types (STs), among which ST-4 (61.5%, 16/26) was predominant, followed by ST-10844 (34.6%, 9/26) and ST-316 (3.8%, 1/26). A total of 21 isolates (80.8%) harbored multidrug resistance (MDR). They showed AMR phenotypes to ampicillin (76.9%, 20/26), cefotaxime (26.9%, 7/26), and ciprofloxacin (69.2%, 18/26; including three ciprofloxacin-intermediate isolates), corresponding to AMR genes and/or chromosomal point mutations of β-lactams (76.9%, 20/26) and fluoroquinolones (100%, 26/26). All ST-10844 isolates possessed MDR, with higher proportions of resistance to cefotaxime and tetracycline. The corresponding AMR genes were mainly carried by two plasmids, IncHI2 and pKPC-CAV1321. The number of virulence genes among the S. Montevideo genomes ranged from 151 to 153, with type III secretion system genes (T3SS; n = 86) predominant. The ranges of the number of prophages, Salmonella Pathogenic Islands (SPIs), plasmid replicons, and MGEs were 2-4, 8-10, 0-5, 17-30, respectively. Phylogenetic analysis showed that global S. Montevideo strains can be divided into five clades, including a novel clade, clade V. Most Chinese isolates (96.6%, 28/29) were assigned to clade II. All the ST-10,844 isolates were from mainland China and assigned to clade II, constituting a distinct cluster.

This study is the first report to characterize S. Montevideo genomes from China. The phenotypic and genomic characteristics of Chinese S. Montevideo isolates were distinct from isolates of other countries, standing out with MDR and tending to be waterborne. A ST-10844 cluster was identified, with higher frequencies of resistance to cefotaxime and tetracycline.