Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection

Abstract Salmonella enterica is a frequent cause of foodborne diseases, which is attributed to its adaptability. Even within a single host, expressing a gene can be beneficial in certain infection stages but neutral or even detrimental in others as previously shown for flagellins. Mutants deficient...

Full description

Saved in:
Bibliographic Details
Main Authors: Noemi Santamaria de Souza, Yassine Cherrak, Thea Bill Andersen, Michel Vetsch, Manja Barthel, Sanne Kroon, Erik Bakkeren, Christopher Schubert, Philipp Christen, Patrick Kiefer, Julia A. Vorholt, Bidong D. Nguyen, Wolf-Dietrich Hardt
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56851-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850029699605987328
author Noemi Santamaria de Souza
Yassine Cherrak
Thea Bill Andersen
Michel Vetsch
Manja Barthel
Sanne Kroon
Erik Bakkeren
Christopher Schubert
Philipp Christen
Patrick Kiefer
Julia A. Vorholt
Bidong D. Nguyen
Wolf-Dietrich Hardt
author_facet Noemi Santamaria de Souza
Yassine Cherrak
Thea Bill Andersen
Michel Vetsch
Manja Barthel
Sanne Kroon
Erik Bakkeren
Christopher Schubert
Philipp Christen
Patrick Kiefer
Julia A. Vorholt
Bidong D. Nguyen
Wolf-Dietrich Hardt
author_sort Noemi Santamaria de Souza
collection DOAJ
description Abstract Salmonella enterica is a frequent cause of foodborne diseases, which is attributed to its adaptability. Even within a single host, expressing a gene can be beneficial in certain infection stages but neutral or even detrimental in others as previously shown for flagellins. Mutants deficient for the conserved glycerol-3-phosphate and phosphate antiporter glpT have been shown to be positively selected in nature, clinical, and laboratory settings. This suggests that different selective pressures select for the presence or absence of GlpT in a context dependent fashion, a phenomenon known as antagonistic pleiotropy. Using mutant libraries and reporters, we investigated the fitness of glpT-deficient mutants during murine orogastric infection. While glpT-deficient mutants thrive during initial growth in the gut lumen, where GlpT’s capacity to import phosphate is disadvantageous, they are counter-selected by macrophages. The dichotomy showcases the need to study the spatial and temporal heterogeneity of enteric pathogens’ fitness across distinct lifestyles and niches. Insights into the differential adaptation during infection may reveal opportunities for therapeutic interventions.
format Article
id doaj-art-682a2971f89c44cdbf315c11995cbda2
institution DOAJ
issn 2041-1723
language English
publishDate 2025-02-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-682a2971f89c44cdbf315c11995cbda22025-08-20T02:59:28ZengNature PortfolioNature Communications2041-17232025-02-0116111910.1038/s41467-025-56851-5Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infectionNoemi Santamaria de Souza0Yassine Cherrak1Thea Bill Andersen2Michel Vetsch3Manja Barthel4Sanne Kroon5Erik Bakkeren6Christopher Schubert7Philipp Christen8Patrick Kiefer9Julia A. Vorholt10Bidong D. Nguyen11Wolf-Dietrich Hardt12Department of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichSir William Dunn School of Pathology, University of OxfordDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichDepartment of Biology, Institute of Microbiology, ETH ZürichAbstract Salmonella enterica is a frequent cause of foodborne diseases, which is attributed to its adaptability. Even within a single host, expressing a gene can be beneficial in certain infection stages but neutral or even detrimental in others as previously shown for flagellins. Mutants deficient for the conserved glycerol-3-phosphate and phosphate antiporter glpT have been shown to be positively selected in nature, clinical, and laboratory settings. This suggests that different selective pressures select for the presence or absence of GlpT in a context dependent fashion, a phenomenon known as antagonistic pleiotropy. Using mutant libraries and reporters, we investigated the fitness of glpT-deficient mutants during murine orogastric infection. While glpT-deficient mutants thrive during initial growth in the gut lumen, where GlpT’s capacity to import phosphate is disadvantageous, they are counter-selected by macrophages. The dichotomy showcases the need to study the spatial and temporal heterogeneity of enteric pathogens’ fitness across distinct lifestyles and niches. Insights into the differential adaptation during infection may reveal opportunities for therapeutic interventions.https://doi.org/10.1038/s41467-025-56851-5
spellingShingle Noemi Santamaria de Souza
Yassine Cherrak
Thea Bill Andersen
Michel Vetsch
Manja Barthel
Sanne Kroon
Erik Bakkeren
Christopher Schubert
Philipp Christen
Patrick Kiefer
Julia A. Vorholt
Bidong D. Nguyen
Wolf-Dietrich Hardt
Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
Nature Communications
title Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
title_full Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
title_fullStr Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
title_full_unstemmed Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
title_short Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection
title_sort context dependent change in the fitness effect of in organic phosphate antiporter glpt during salmonella typhimurium infection
url https://doi.org/10.1038/s41467-025-56851-5
work_keys_str_mv AT noemisantamariadesouza contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT yassinecherrak contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT theabillandersen contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT michelvetsch contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT manjabarthel contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT sannekroon contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT erikbakkeren contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT christopherschubert contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT philippchristen contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT patrickkiefer contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT juliaavorholt contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT bidongdnguyen contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection
AT wolfdietrichhardt contextdependentchangeinthefitnesseffectofinorganicphosphateantiporterglptduringsalmonellatyphimuriuminfection