Cargando…

A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum

Bacterial pathogenicity relies on a proficient metabolism and there is increasing evidence that metabolic adaptation to exploit host resources is a key property of infectious organisms. In many cases, colonization by the pathogen also implies an intensive multiplication and the necessity to produce...

Descripción completa

Detalles Bibliográficos
Autores principales: Peyraud, Rémi, Cottret, Ludovic, Marmiesse, Lucas, Gouzy, Jérôme, Genin, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5061431/
https://www.ncbi.nlm.nih.gov/pubmed/27732672
http://dx.doi.org/10.1371/journal.ppat.1005939
_version_ 1782459605711847424
author Peyraud, Rémi
Cottret, Ludovic
Marmiesse, Lucas
Gouzy, Jérôme
Genin, Stéphane
author_facet Peyraud, Rémi
Cottret, Ludovic
Marmiesse, Lucas
Gouzy, Jérôme
Genin, Stéphane
author_sort Peyraud, Rémi
collection PubMed
description Bacterial pathogenicity relies on a proficient metabolism and there is increasing evidence that metabolic adaptation to exploit host resources is a key property of infectious organisms. In many cases, colonization by the pathogen also implies an intensive multiplication and the necessity to produce a large array of virulence factors, which may represent a significant cost for the pathogen. We describe here the existence of a resource allocation trade-off mechanism in the plant pathogen R. solanacearum. We generated a genome-scale reconstruction of the metabolic network of R. solanacearum, together with a macromolecule network module accounting for the production and secretion of hundreds of virulence determinants. By using a combination of constraint-based modeling and metabolic flux analyses, we quantified the metabolic cost for production of exopolysaccharides, which are critical for disease symptom production, and other virulence factors. We demonstrated that this trade-off between virulence factor production and bacterial proliferation is controlled by the quorum-sensing-dependent regulatory protein PhcA. A phcA mutant is avirulent but has a better growth rate than the wild-type strain. Moreover, a phcA mutant has an expanded metabolic versatility, being able to metabolize 17 substrates more than the wild-type. Model predictions indicate that metabolic pathways are optimally oriented towards proliferation in a phcA mutant and we show that this enhanced metabolic versatility in phcA mutants is to a large extent a consequence of not paying the cost for virulence. This analysis allowed identifying candidate metabolic substrates having a substantial impact on bacterial growth during infection. Interestingly, the substrates supporting well both production of virulence factors and growth are those found in higher amount within the plant host. These findings also provide an explanatory basis to the well-known emergence of avirulent variants in R. solanacearum populations in planta or in stressful environments.
format Online
Article
Text
id pubmed-5061431
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-50614312016-10-27 A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum Peyraud, Rémi Cottret, Ludovic Marmiesse, Lucas Gouzy, Jérôme Genin, Stéphane PLoS Pathog Research Article Bacterial pathogenicity relies on a proficient metabolism and there is increasing evidence that metabolic adaptation to exploit host resources is a key property of infectious organisms. In many cases, colonization by the pathogen also implies an intensive multiplication and the necessity to produce a large array of virulence factors, which may represent a significant cost for the pathogen. We describe here the existence of a resource allocation trade-off mechanism in the plant pathogen R. solanacearum. We generated a genome-scale reconstruction of the metabolic network of R. solanacearum, together with a macromolecule network module accounting for the production and secretion of hundreds of virulence determinants. By using a combination of constraint-based modeling and metabolic flux analyses, we quantified the metabolic cost for production of exopolysaccharides, which are critical for disease symptom production, and other virulence factors. We demonstrated that this trade-off between virulence factor production and bacterial proliferation is controlled by the quorum-sensing-dependent regulatory protein PhcA. A phcA mutant is avirulent but has a better growth rate than the wild-type strain. Moreover, a phcA mutant has an expanded metabolic versatility, being able to metabolize 17 substrates more than the wild-type. Model predictions indicate that metabolic pathways are optimally oriented towards proliferation in a phcA mutant and we show that this enhanced metabolic versatility in phcA mutants is to a large extent a consequence of not paying the cost for virulence. This analysis allowed identifying candidate metabolic substrates having a substantial impact on bacterial growth during infection. Interestingly, the substrates supporting well both production of virulence factors and growth are those found in higher amount within the plant host. These findings also provide an explanatory basis to the well-known emergence of avirulent variants in R. solanacearum populations in planta or in stressful environments. Public Library of Science 2016-10-12 /pmc/articles/PMC5061431/ /pubmed/27732672 http://dx.doi.org/10.1371/journal.ppat.1005939 Text en © 2016 Peyraud 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
Peyraud, Rémi
Cottret, Ludovic
Marmiesse, Lucas
Gouzy, Jérôme
Genin, Stéphane
A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title_full A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title_fullStr A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title_full_unstemmed A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title_short A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum
title_sort resource allocation trade-off between virulence and proliferation drives metabolic versatility in the plant pathogen ralstonia solanacearum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5061431/
https://www.ncbi.nlm.nih.gov/pubmed/27732672
http://dx.doi.org/10.1371/journal.ppat.1005939
work_keys_str_mv AT peyraudremi aresourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT cottretludovic aresourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT marmiesselucas aresourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT gouzyjerome aresourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT geninstephane aresourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT peyraudremi resourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT cottretludovic resourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT marmiesselucas resourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT gouzyjerome resourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum
AT geninstephane resourceallocationtradeoffbetweenvirulenceandproliferationdrivesmetabolicversatilityintheplantpathogenralstoniasolanacearum