Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health

Abstract Salmonella enterica variants exhibit diverse host adaptation, outcome of infection, and associated risk to food safety. Analysis of the distribution of Salmonella enterica serovar Derby (S. Derby) subtypes in human and swine identified isolates with a distinct PFGE profile that were signifi...

Full description

Bibliographic Details
Main Authors: Martina Tambassi, Melissa Berni, Chiara Bracchi, Erika Scaltriti, Marina Morganti, Luca Bolzoni, Jennifer R. Tanner, Gaëtan Thilliez, Robert A. Kingsley, Stefano Pongolini, Gabriele Casadei
Format: Article
Language:English
Published: Nature Portfolio 2020-12-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-78443-7
_version_ 1818429992349990912
author Martina Tambassi
Melissa Berni
Chiara Bracchi
Erika Scaltriti
Marina Morganti
Luca Bolzoni
Jennifer R. Tanner
Gaëtan Thilliez
Robert A. Kingsley
Stefano Pongolini
Gabriele Casadei
author_facet Martina Tambassi
Melissa Berni
Chiara Bracchi
Erika Scaltriti
Marina Morganti
Luca Bolzoni
Jennifer R. Tanner
Gaëtan Thilliez
Robert A. Kingsley
Stefano Pongolini
Gabriele Casadei
author_sort Martina Tambassi
collection DOAJ
description Abstract Salmonella enterica variants exhibit diverse host adaptation, outcome of infection, and associated risk to food safety. Analysis of the distribution of Salmonella enterica serovar Derby (S. Derby) subtypes in human and swine identified isolates with a distinct PFGE profile that were significantly under-represented in human infections, consistent with further host adaptation to swine. Here we show that isolates with this PFGE profile form a distinct phylogenetic sub-clade within S. Derby and exhibit a profound reduction in invasion of human epithelial cells, and a relatively small reduction in swine epithelial cells. A single missense mutation in hilD, that encodes the master-regulator of the Salmonella Pathogenicity Island 1 (SPI-1), was present in the adapted lineage. The missense mutation resulted in a loss of function of HilD that accounted for reduced invasion in human epithelial cells. The relatively small impact of the mutation on interaction with swine cells was consistent with an alternative mechanism of invasion in this pathogen-host combination.
first_indexed 2024-12-14T15:26:19Z
format Article
id doaj.art-129ad161b59b4c36a5a84aad6931a6d0
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-14T15:26:19Z
publishDate 2020-12-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-129ad161b59b4c36a5a84aad6931a6d02022-12-21T22:56:00ZengNature PortfolioScientific Reports2045-23222020-12-0110111310.1038/s41598-020-78443-7Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human healthMartina Tambassi0Melissa Berni1Chiara Bracchi2Erika Scaltriti3Marina Morganti4Luca Bolzoni5Jennifer R. Tanner6Gaëtan Thilliez7Robert A. Kingsley8Stefano Pongolini9Gabriele Casadei10Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaQuadram Institute BioscienceQuadram Institute BioscienceQuadram Institute BioscienceRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaRisk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia RomagnaAbstract Salmonella enterica variants exhibit diverse host adaptation, outcome of infection, and associated risk to food safety. Analysis of the distribution of Salmonella enterica serovar Derby (S. Derby) subtypes in human and swine identified isolates with a distinct PFGE profile that were significantly under-represented in human infections, consistent with further host adaptation to swine. Here we show that isolates with this PFGE profile form a distinct phylogenetic sub-clade within S. Derby and exhibit a profound reduction in invasion of human epithelial cells, and a relatively small reduction in swine epithelial cells. A single missense mutation in hilD, that encodes the master-regulator of the Salmonella Pathogenicity Island 1 (SPI-1), was present in the adapted lineage. The missense mutation resulted in a loss of function of HilD that accounted for reduced invasion in human epithelial cells. The relatively small impact of the mutation on interaction with swine cells was consistent with an alternative mechanism of invasion in this pathogen-host combination.https://doi.org/10.1038/s41598-020-78443-7
spellingShingle Martina Tambassi
Melissa Berni
Chiara Bracchi
Erika Scaltriti
Marina Morganti
Luca Bolzoni
Jennifer R. Tanner
Gaëtan Thilliez
Robert A. Kingsley
Stefano Pongolini
Gabriele Casadei
Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
Scientific Reports
title Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
title_full Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
title_fullStr Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
title_full_unstemmed Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
title_short Mutation of hilD in a Salmonella Derby lineage linked to swine adaptation and reduced risk to human health
title_sort mutation of hild in a salmonella derby lineage linked to swine adaptation and reduced risk to human health
url https://doi.org/10.1038/s41598-020-78443-7
work_keys_str_mv AT martinatambassi mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT melissaberni mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT chiarabracchi mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT erikascaltriti mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT marinamorganti mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT lucabolzoni mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT jenniferrtanner mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT gaetanthilliez mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT robertakingsley mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT stefanopongolini mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth
AT gabrielecasadei mutationofhildinasalmonelladerbylineagelinkedtoswineadaptationandreducedrisktohumanhealth