Genomic epidemiology and multilevel genome typing of Australian Salmonella enterica serovar Enteritidis
Authors: Luo Lijuan , Payne Michael , Wang Qinning , Kaur Sandeep , Rathnayake Irani U. , Graham Rikki , Gall Mailie , Draper Jenny , Martinez Elena , Octavia Sophie , Tanaka Mark M. , Jennison Amy V. , Sintchenko Vitali , Lan Ruiting 
Published: May 2022

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.