Genomic epidemiology and multilevel genome typing of Australian Salmonella enterica serovar Enteritidis

Salmonella enterica serovar Enteritidis is one of the leading causes of salmonellosis in Australia. However, the majority of S . Enteritidis cases in Australia are travel-related with a small proportion being locally acquired. This study aimed to characterise the genomic features of Australian S . Enteritidis and compare them with international strains using multilevel genome typing (MGT). A total of 568 S . Enteritidis isolates from two Australian states across two consecutive years were analysed using the S . Enteritidis MGT scheme and database (MGTdb) - which contained 40,390 publicly available genomes from 99 countries. The Australian S . Enteritidis strains were divided into three phylogenetic clades (A, B and C). Clades A and C represented 16.4% and 3.5% of the total isolates, respectively, and were of local origin. Clade B accounted for 80.1% of the isolates which belonged to seven previously defined lineages but was dominated by the global epidemic lineage (MGT4-CC1). At MGT5 level, three out of five top sequence types (STs) in Australia were also top STs in Asia, suggesting that a fair proportion of Australian S . Enteritidis cases may be epidemiologically linked with Asian strains. In 2018, a large egg-associated local outbreak was caused by a recently defined clade B lineage prevalent in Europe and was closely related, but not directly linked, to three isolates from Europe. Additionally, antimicrobial-resistance genes were only found in Australian clade B isolates, with a predicted multidrug resistance (MDR) rate of 11.7%. Over half (54.8%) of the MDR isolates belonged to 10 MDR-associated MGT-STs, which were also frequent in Asian S . Enteritidis. IncX1 plasmids were frequently present in the Australian MDR isolates. Overall, this study investigated the genomic epidemiology of S . Enteritidis in Australia, including the first large local outbreak, using MGT. The open MGT platform enables a standardised and sharable nomenclature that can be effectively applied to public health for unified surveillance of S . Enteritidis nationally and globally. Importance Salmonella enterica serovar Enteritidis is a leading cause of foodborne infections. We previously developed a genomic typing database – MGTdb for S . Enteritidis to facilitate global surveillance of this pathogen. In this study we examined the genomic features of Australian S . Enteritidis using the MGTdb and found that Australian S . Enteritidis is mainly epidemiologically linked with Asian strains (especially strains carrying antimicrobial resistance genes) followed by European strains. The first large-scale egg-associated local outbreak in Australia was caused by a recently defined lineage prevalent in Europe, and three European isolates in the MGTdb were closely related but not directly linked to this outbreak. In summary, the S . Enteritidis MGTdb open platform is shown to be a potential powerful tool for national and global public health surveillance of this pathogen.