Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis

ABSTRACT Salmonella enterica serovar Enteritidis is one of the leading causes of salmonellosis in Australia. In this study, a total of 568 S. Enteritidis isolates from two Australian states across two consecutive years were analyzed and compared to international strains, using the S. Enteritidis mul...

Full description

Bibliographic Details
Main Authors: Lijuan Luo, Michael Payne, Qinning Wang, Sandeep Kaur, Irani U. Rathnayake, Rikki Graham, Mailie Gall, Jenny Draper, Elena Martinez, Sophie Octavia, Mark M. Tanaka, Amy V. Jennison, Vitali Sintchenko, Ruiting Lan
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03014-22
_version_ 1811164407963582464
author Lijuan Luo
Michael Payne
Qinning Wang
Sandeep Kaur
Irani U. Rathnayake
Rikki Graham
Mailie Gall
Jenny Draper
Elena Martinez
Sophie Octavia
Mark M. Tanaka
Amy V. Jennison
Vitali Sintchenko
Ruiting Lan
author_facet Lijuan Luo
Michael Payne
Qinning Wang
Sandeep Kaur
Irani U. Rathnayake
Rikki Graham
Mailie Gall
Jenny Draper
Elena Martinez
Sophie Octavia
Mark M. Tanaka
Amy V. Jennison
Vitali Sintchenko
Ruiting Lan
author_sort Lijuan Luo
collection DOAJ
description ABSTRACT Salmonella enterica serovar Enteritidis is one of the leading causes of salmonellosis in Australia. In this study, a total of 568 S. Enteritidis isolates from two Australian states across two consecutive years were analyzed and compared to international strains, using the S. Enteritidis multilevel genome typing (MGT) database, which contained 40,390 publicly available genomes from 99 countries. The Australian S. Enteritidis isolates 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. At the 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 European isolates. Additionally, over half (54.8%) of predicted multidrug resistance (MDR) isolates belonged to 10 MDR-associated MGT-STs, which were also frequent in Asian S. Enteritidis . 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 standardized 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 potentially powerful tool for national and global public health surveillance of this pathogen.
first_indexed 2024-04-10T15:22:06Z
format Article
id doaj.art-ec0fed3056bf4d468c1291f60a25a86e
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-04-10T15:22:06Z
publishDate 2023-02-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-ec0fed3056bf4d468c1291f60a25a86e2023-02-14T14:15:49ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.03014-22Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar EnteritidisLijuan Luo0Michael Payne1Qinning Wang2Sandeep Kaur3Irani U. Rathnayake4Rikki Graham5Mailie Gall6Jenny Draper7Elena Martinez8Sophie Octavia9Mark M. Tanaka10Amy V. Jennison11Vitali Sintchenko12Ruiting Lan13School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaCentre for Infectious Diseases and Microbiology–Public Health, Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaPublic Health Microbiology, Forensic and Scientific Services, Queensland Department of Health, Coopers Plains, Queensland, AustraliaPublic Health Microbiology, Forensic and Scientific Services, Queensland Department of Health, Coopers Plains, Queensland, AustraliaCentre for Infectious Diseases and Microbiology–Public Health, Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, AustraliaCentre for Infectious Diseases and Microbiology–Public Health, Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, AustraliaCentre for Infectious Diseases and Microbiology–Public Health, Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaPublic Health Microbiology, Forensic and Scientific Services, Queensland Department of Health, Coopers Plains, Queensland, AustraliaCentre for Infectious Diseases and Microbiology–Public Health, Institute of Clinical Pathology and Medical Research–NSW Health Pathology, Westmead Hospital, Westmead, New South Wales, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, AustraliaABSTRACT Salmonella enterica serovar Enteritidis is one of the leading causes of salmonellosis in Australia. In this study, a total of 568 S. Enteritidis isolates from two Australian states across two consecutive years were analyzed and compared to international strains, using the S. Enteritidis multilevel genome typing (MGT) database, which contained 40,390 publicly available genomes from 99 countries. The Australian S. Enteritidis isolates 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. At the 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 European isolates. Additionally, over half (54.8%) of predicted multidrug resistance (MDR) isolates belonged to 10 MDR-associated MGT-STs, which were also frequent in Asian S. Enteritidis . 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 standardized 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 potentially powerful tool for national and global public health surveillance of this pathogen.https://journals.asm.org/doi/10.1128/spectrum.03014-22Salmonella Enteritidisgenomic epidemiologyfoodborne outbreakmultilevel genome typingstandardized genomic typinggenomic typing database
spellingShingle Lijuan Luo
Michael Payne
Qinning Wang
Sandeep Kaur
Irani U. Rathnayake
Rikki Graham
Mailie Gall
Jenny Draper
Elena Martinez
Sophie Octavia
Mark M. Tanaka
Amy V. Jennison
Vitali Sintchenko
Ruiting Lan
Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
Microbiology Spectrum
Salmonella Enteritidis
genomic epidemiology
foodborne outbreak
multilevel genome typing
standardized genomic typing
genomic typing database
title Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
title_full Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
title_fullStr Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
title_full_unstemmed Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
title_short Genomic Epidemiology and Multilevel Genome Typing of Australian Salmonella enterica Serovar Enteritidis
title_sort genomic epidemiology and multilevel genome typing of australian salmonella enterica serovar enteritidis
topic Salmonella Enteritidis
genomic epidemiology
foodborne outbreak
multilevel genome typing
standardized genomic typing
genomic typing database
url https://journals.asm.org/doi/10.1128/spectrum.03014-22
work_keys_str_mv AT lijuanluo genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT michaelpayne genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT qinningwang genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT sandeepkaur genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT iraniurathnayake genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT rikkigraham genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT mailiegall genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT jennydraper genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT elenamartinez genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT sophieoctavia genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT markmtanaka genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT amyvjennison genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT vitalisintchenko genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis
AT ruitinglan genomicepidemiologyandmultilevelgenometypingofaustraliansalmonellaentericaserovarenteritidis