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Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence

Pathogen access to host nutrients in infected tissues is fundamental for pathogen growth and virulence, disease progression, and infection control. However, our understanding of this crucial process is still rather limited because of experimental and conceptual challenges. Here, we used proteomics,...

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Autores principales: Steeb, Benjamin, Claudi, Beatrice, Burton, Neil A., Tienz, Petra, Schmidt, Alexander, Farhan, Hesso, Mazé, Alain, Bumann, Dirk
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636032/
https://www.ncbi.nlm.nih.gov/pubmed/23633950
http://dx.doi.org/10.1371/journal.ppat.1003301
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author Steeb, Benjamin
Claudi, Beatrice
Burton, Neil A.
Tienz, Petra
Schmidt, Alexander
Farhan, Hesso
Mazé, Alain
Bumann, Dirk
author_facet Steeb, Benjamin
Claudi, Beatrice
Burton, Neil A.
Tienz, Petra
Schmidt, Alexander
Farhan, Hesso
Mazé, Alain
Bumann, Dirk
author_sort Steeb, Benjamin
collection PubMed
description Pathogen access to host nutrients in infected tissues is fundamental for pathogen growth and virulence, disease progression, and infection control. However, our understanding of this crucial process is still rather limited because of experimental and conceptual challenges. Here, we used proteomics, microbial genetics, competitive infections, and computational approaches to obtain a comprehensive overview of Salmonella nutrition and growth in a mouse typhoid fever model. The data revealed that Salmonella accessed an unexpectedly diverse set of at least 31 different host nutrients in infected tissues but the individual nutrients were available in only scarce amounts. Salmonella adapted to this situation by expressing versatile catabolic pathways to simultaneously exploit multiple host nutrients. A genome-scale computational model of Salmonella in vivo metabolism based on these data was fully consistent with independent large-scale experimental data on Salmonella enzyme quantities, and correctly predicted 92% of 738 reported experimental mutant virulence phenotypes, suggesting that our analysis provided a comprehensive overview of host nutrient supply, Salmonella metabolism, and Salmonella growth during infection. Comparison of metabolic networks of other pathogens suggested that complex host/pathogen nutritional interfaces are a common feature underlying many infectious diseases.
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spelling pubmed-36360322013-04-30 Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence Steeb, Benjamin Claudi, Beatrice Burton, Neil A. Tienz, Petra Schmidt, Alexander Farhan, Hesso Mazé, Alain Bumann, Dirk PLoS Pathog Research Article Pathogen access to host nutrients in infected tissues is fundamental for pathogen growth and virulence, disease progression, and infection control. However, our understanding of this crucial process is still rather limited because of experimental and conceptual challenges. Here, we used proteomics, microbial genetics, competitive infections, and computational approaches to obtain a comprehensive overview of Salmonella nutrition and growth in a mouse typhoid fever model. The data revealed that Salmonella accessed an unexpectedly diverse set of at least 31 different host nutrients in infected tissues but the individual nutrients were available in only scarce amounts. Salmonella adapted to this situation by expressing versatile catabolic pathways to simultaneously exploit multiple host nutrients. A genome-scale computational model of Salmonella in vivo metabolism based on these data was fully consistent with independent large-scale experimental data on Salmonella enzyme quantities, and correctly predicted 92% of 738 reported experimental mutant virulence phenotypes, suggesting that our analysis provided a comprehensive overview of host nutrient supply, Salmonella metabolism, and Salmonella growth during infection. Comparison of metabolic networks of other pathogens suggested that complex host/pathogen nutritional interfaces are a common feature underlying many infectious diseases. Public Library of Science 2013-04-25 /pmc/articles/PMC3636032/ /pubmed/23633950 http://dx.doi.org/10.1371/journal.ppat.1003301 Text en © 2013 Steeb et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Steeb, Benjamin
Claudi, Beatrice
Burton, Neil A.
Tienz, Petra
Schmidt, Alexander
Farhan, Hesso
Mazé, Alain
Bumann, Dirk
Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title_full Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title_fullStr Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title_full_unstemmed Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title_short Parallel Exploitation of Diverse Host Nutrients Enhances Salmonella Virulence
title_sort parallel exploitation of diverse host nutrients enhances salmonella virulence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636032/
https://www.ncbi.nlm.nih.gov/pubmed/23633950
http://dx.doi.org/10.1371/journal.ppat.1003301
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