Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin
Salmonella Dublin is a host-adapted, invasive nontyphoidal Salmonella (iNTS) serovar that causes bloodstream infections in humans and demonstrates increasing prevalence of antimicrobial resistance (AMR). Using a global dataset of 1303 genomes, coupled with in vitro assays, we examined the evolutiona...
Saved in:
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2025-06-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/102253 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1839652288980844544 |
|---|---|
| author | Cheryll M Sia Rebecca L Ambrose Mary Valcanis Patiyan Andersson Susan A Ballard Benjamin P Howden Deborah A Williamson Jaclyn S Pearson Danielle J Ingle |
| author_facet | Cheryll M Sia Rebecca L Ambrose Mary Valcanis Patiyan Andersson Susan A Ballard Benjamin P Howden Deborah A Williamson Jaclyn S Pearson Danielle J Ingle |
| author_sort | Cheryll M Sia |
| collection | DOAJ |
| description | Salmonella Dublin is a host-adapted, invasive nontyphoidal Salmonella (iNTS) serovar that causes bloodstream infections in humans and demonstrates increasing prevalence of antimicrobial resistance (AMR). Using a global dataset of 1303 genomes, coupled with in vitro assays, we examined the evolutionary, resistance, and virulence characteristics of S. Dublin. Our analysis revealed strong geographical associations between AMR profiles and plasmid types, with highly resistant isolates confined predominantly to North America, linked to IncC plasmids co-encoding AMR and heavy metal resistance. By contrast, Australian isolates were largely antimicrobial-susceptible, reflecting differing AMR pressures. We identified two phylogenetically distinct Australian lineages, ST10 and ST74, with a small number of ST10 isolates harbouring a novel hybrid plasmid encoding both AMR and mercuric resistance. Whereas the ST10 lineage remains globally dominant, the ST74 lineage was less prevalent. ST74 exhibited unique genomic features including a larger pan genome compared to ST10 and the absence of key virulence loci, including Salmonella pathogenicity island (SPI)-19 which encodes a type VI secretion system (T6SS). Despite these genomic differences, the ST74 lineage displayed enhanced intracellular replication in human macrophages and induced less pro-inflammatory responses compared with ST10, suggesting alternative virulence strategies that may support systemic dissemination of ST74. The Vi antigen was absent in all ST10 and ST74 genomes, highlighting challenges for serotyping and vaccine development, and has implications for current diagnostic and control strategies for S. Dublin infections. Collectively, this study represents the most comprehensive investigation of S. Dublin to date and, importantly, has revealed distinct adaptations of two genotypes within the same serovar, leading to different epidemiological success. The regional emergence and evolution of distinct S. Dublin lineages highlight the need to understand the divergence of intra-serovar virulence mechanisms which may impact the development of effective control measures against this important global pathogen. |
| format | Article |
| id | doaj-art-ec8f1fa8afb3492b9ef7cac9feb9ce6b |
| institution | Matheson Library |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-ec8f1fa8afb3492b9ef7cac9feb9ce6b2025-06-25T15:51:55ZengeLife Sciences Publications LtdeLife2050-084X2025-06-011310.7554/eLife.102253Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar DublinCheryll M Sia0https://orcid.org/0000-0002-7058-6022Rebecca L Ambrose1Mary Valcanis2Patiyan Andersson3Susan A Ballard4Benjamin P Howden5https://orcid.org/0000-0003-0237-1473Deborah A Williamson6Jaclyn S Pearson7https://orcid.org/0000-0002-7358-4479Danielle J Ingle8https://orcid.org/0000-0003-0707-6537Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia; Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaCentre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research, Clayton, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaMicrobiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaDepartment of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, Australia; Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaSchool of Medicine, University of St Andrews, St Andrews, United KingdomCentre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research, Clayton, Australia; School of Medicine, University of St Andrews, St Andrews, United Kingdom; Department of Microbiology, Monash University, Clayton, AustraliaDepartment of Microbiology and Immunology, The University of Melbourne at The Peter Doherty Institute for Infection and Immunity, Melbourne, AustraliaSalmonella Dublin is a host-adapted, invasive nontyphoidal Salmonella (iNTS) serovar that causes bloodstream infections in humans and demonstrates increasing prevalence of antimicrobial resistance (AMR). Using a global dataset of 1303 genomes, coupled with in vitro assays, we examined the evolutionary, resistance, and virulence characteristics of S. Dublin. Our analysis revealed strong geographical associations between AMR profiles and plasmid types, with highly resistant isolates confined predominantly to North America, linked to IncC plasmids co-encoding AMR and heavy metal resistance. By contrast, Australian isolates were largely antimicrobial-susceptible, reflecting differing AMR pressures. We identified two phylogenetically distinct Australian lineages, ST10 and ST74, with a small number of ST10 isolates harbouring a novel hybrid plasmid encoding both AMR and mercuric resistance. Whereas the ST10 lineage remains globally dominant, the ST74 lineage was less prevalent. ST74 exhibited unique genomic features including a larger pan genome compared to ST10 and the absence of key virulence loci, including Salmonella pathogenicity island (SPI)-19 which encodes a type VI secretion system (T6SS). Despite these genomic differences, the ST74 lineage displayed enhanced intracellular replication in human macrophages and induced less pro-inflammatory responses compared with ST10, suggesting alternative virulence strategies that may support systemic dissemination of ST74. The Vi antigen was absent in all ST10 and ST74 genomes, highlighting challenges for serotyping and vaccine development, and has implications for current diagnostic and control strategies for S. Dublin infections. Collectively, this study represents the most comprehensive investigation of S. Dublin to date and, importantly, has revealed distinct adaptations of two genotypes within the same serovar, leading to different epidemiological success. The regional emergence and evolution of distinct S. Dublin lineages highlight the need to understand the divergence of intra-serovar virulence mechanisms which may impact the development of effective control measures against this important global pathogen.https://elifesciences.org/articles/102253Salmonella Dublinepidemiologyhost immune responseinvasive nontyphoidal Salmonella |
| spellingShingle | Cheryll M Sia Rebecca L Ambrose Mary Valcanis Patiyan Andersson Susan A Ballard Benjamin P Howden Deborah A Williamson Jaclyn S Pearson Danielle J Ingle Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin eLife Salmonella Dublin epidemiology host immune response invasive nontyphoidal Salmonella |
| title | Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin |
| title_full | Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin |
| title_fullStr | Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin |
| title_full_unstemmed | Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin |
| title_short | Distinct adaptation and epidemiological success of different genotypes within Salmonella enterica serovar Dublin |
| title_sort | distinct adaptation and epidemiological success of different genotypes within salmonella enterica serovar dublin |
| topic | Salmonella Dublin epidemiology host immune response invasive nontyphoidal Salmonella |
| url | https://elifesciences.org/articles/102253 |
| work_keys_str_mv | AT cheryllmsia distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT rebeccalambrose distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT maryvalcanis distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT patiyanandersson distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT susanaballard distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT benjaminphowden distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT deborahawilliamson distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT jaclynspearson distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin AT daniellejingle distinctadaptationandepidemiologicalsuccessofdifferentgenotypeswithinsalmonellaentericaserovardublin |