Genomic and resistome analysis of Salmonella enterica isolates from retail markets in Yichun city, China

Abstract

Nontyphoidal Salmonella (NTS) causes global outbreaks of foodborne disease. The main source of Salmonella for humans is animal-borne foods; however, the monitoring of Salmonella in the food chain via genomic platforms was limited in China. This study evaluated the prevalence, resistome, and virulome diversity of Salmonella strains identified from pork, retail environment, aquatic products, and poultry eggs of retail markets in Yichun city, Jiangxi province. The overall incidence of Salmonella was 9.4 %, with a higher contamination rate observed in pork at 13.5 %, followed by the retail environment at 7.69 %. The genomic analysis of the isolates revealed a total of fifteen distinct serovars, with serovar Enteritidis being the most prevalent (64.3 %). The phenotypic resistance analysis conducted by the broth microdilution method, revealed that 81.12 % of the isolates exhibited multidrug resistance (MDR), with high resistance to trimethoprim/sulphonamides (100 %), followed by tetracycline (99.3 %) and streptomycin (99.3 %). Genotypic analysis of antimicrobial resistance identified 80 antimicrobial-resistant genes (ARGs), with mdf(A), aph(3')-Ib, tet(A), dfrA12, floR, bla _TEM-1B , qnrS3, and sul2, conferring resistance to different antimicrobial classes, being the predominant ARGs. Additionally, forty ESBL genes, particularly critical genes such as bla _CTX-M and bla _NDM-1, were also identified in Salmonella isolates. The IncR, IncFIB (K), and IncX1 plasmid replicons were widely prevalent and served as significant reservoirs of horizontally acquired foreign genes. Moreover, key virulence genes such as cdtB, lpf and sef were also detected, in addition to Salmonella pathogenicity islands SPI-1 and SPI-2. This study reveals the prevalence of multidrug-resistant and virulent strains of Salmonella serovars in the markets of Yichuan city, posing a risk of human infections. The gained knowledge provided essential baseline information that may be utilized for regular tracking of MDR Salmonella transmission in the food chain to minimize potential future outbreaks.

Keywords: One health; Pork; Resistome; Retail environment; Salmonella.

Fig. 1

A Sankey diagram demonstrating the temporal distribution of Salmonella serovars among pork, aquatic products, poultry eggs and retail environmental sources in Yichun. The diameter of the line is proportional to the number of isolates from a given source.

Fig. 2

Summary of overall resistance percentages of Salmonella isolates (n = 143) to different types of antibiotics determined by the broth microdilution method. (a): The individual AMR percentage of Salmonella tested with 13 antibiotics. (b): Percentage of Salmonella isolates found to be MDR and PDR in our study. (c): MDR and PDR Salmonella isolates were found in pork, the environment, aquatic products, and poultry eggs.

Fig. 3

Antimicrobial resistance pattern of 143 strains of Salmonella enterica isolated from different sources. (a, b): Different antimicrobial resistance patterns of all 143 Salmonella isolates according to sample sources. (c): The heatmap shows AMR profiles grouped by the drug class to which Salmonella strains isolated from pork, environment, aquaculture, and poultry eggs in China were phenotypically resistant.

Fig. 4

The distribution of antimicrobial resistance genes (ARGs) belongs to different antimicrobial classes among 143 Salmonella isolates from veterinary and environmental sources. Genes detected in the genomes associated with AMR are shown on the y-axis of the graph and are grouped by drug class. The dark blue color in the heatmap represents the presence of ARGs and light blue color indicates the absence of ARGs. The strain names were shown at the top. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

Distribution of plasmid replicons among Salmonella strains isolated from different sources.

Fig. 6

Co-occurrence of common plasmid replicons, top ten detected AMR-associated genes and invasive index of Salmonella isolates from different sources. (a): The primary source of ARGs is carried by distinct plasmid replicons. The connecting line between ARGs and plasmid replicons represents the potential carrying relationship. (b): The box plot graph showed the invasive index of Salmonella isolates from different sources. Isolates from poultry eggs are less invasive. No statistical differences were observed among isolates from different sources.

Fig. 7

Distribution of virulence genes among the studied isolates. The color of the individual cells varies with the prevalence of each virulence gene.