Cargando…

Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex

All the strains grouped under the species Ralstonia solanacearum represent a species complex responsible for many diseases on agricultural crops throughout the world. The strains have different lifestyles and host range. Here, we investigated whether specific metabolic pathways contribute to strain...

Descripción completa

Detalles Bibliográficos
Autores principales: Baroukh, Caroline, Cottret, Ludovic, Pires, Emma, Peyraud, Rémi, Guidot, Alice, Genin, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470067/
https://www.ncbi.nlm.nih.gov/pubmed/37341493
http://dx.doi.org/10.1128/msystems.00083-23
_version_ 1785099600371122176
author Baroukh, Caroline
Cottret, Ludovic
Pires, Emma
Peyraud, Rémi
Guidot, Alice
Genin, Stéphane
author_facet Baroukh, Caroline
Cottret, Ludovic
Pires, Emma
Peyraud, Rémi
Guidot, Alice
Genin, Stéphane
author_sort Baroukh, Caroline
collection PubMed
description All the strains grouped under the species Ralstonia solanacearum represent a species complex responsible for many diseases on agricultural crops throughout the world. The strains have different lifestyles and host range. Here, we investigated whether specific metabolic pathways contribute to strain diversification. To this end, we carried out systematic comparisons on 11 strains representing the diversity of the species complex. We reconstructed the metabolic network of each strain from its genome sequence and looked for the metabolic pathways differentiating the different reconstructed networks and, by extension, the different strains. Finally, we conducted an experimental validation by determining the metabolic profile of each strain with the Biolog technology. Results revealed that the metabolism is conserved between strains, with a core metabolism composed of 82% of the pan-reactome. The three species composing the species complex could be distinguished according to the presence/absence of some metabolic pathways, in particular, one involving salicylic acid degradation. Phenotypic assays revealed that the trophic preferences on organic acids and several amino acids such as glutamine, glutamate, aspartate, and asparagine are conserved between strains. Finally, we generated mutants lacking the quorum-sensing-dependent regulator PhcA in four diverse strains, and we showed that the phcA-dependent trade-off between growth and production of virulence factors is conserved across the R. solanacearum species complex. IMPORTANCE: Ralstonia solanacearum is one of the most important threats to plant health worldwide, causing disease on a very large range of agricultural crops such as tomato or potato. Behind the R. solanacearum name are hundreds of strains with different host range and lifestyle, classified into three species. Studying the differences between strains allows to better apprehend the biology of the pathogens and the specificity of some strains. None of the published genomic comparative studies have focused on the metabolism of the strains so far. We developed a new bioinformatic pipeline to build high-quality metabolic networks and used a combination of metabolic modeling and high-throughput phenotypic Biolog microplates to look for the metabolic differences between 11 strains across the three species. Our study revealed that genes encoding enzymes are overall conserved, with few variations between strains. However, more variations were observed when considering substrate usage. These variations probably result from regulation rather than the presence or absence of enzymes in the genome.
format Online
Article
Text
id pubmed-10470067
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-104700672023-09-01 Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex Baroukh, Caroline Cottret, Ludovic Pires, Emma Peyraud, Rémi Guidot, Alice Genin, Stéphane mSystems Research Article All the strains grouped under the species Ralstonia solanacearum represent a species complex responsible for many diseases on agricultural crops throughout the world. The strains have different lifestyles and host range. Here, we investigated whether specific metabolic pathways contribute to strain diversification. To this end, we carried out systematic comparisons on 11 strains representing the diversity of the species complex. We reconstructed the metabolic network of each strain from its genome sequence and looked for the metabolic pathways differentiating the different reconstructed networks and, by extension, the different strains. Finally, we conducted an experimental validation by determining the metabolic profile of each strain with the Biolog technology. Results revealed that the metabolism is conserved between strains, with a core metabolism composed of 82% of the pan-reactome. The three species composing the species complex could be distinguished according to the presence/absence of some metabolic pathways, in particular, one involving salicylic acid degradation. Phenotypic assays revealed that the trophic preferences on organic acids and several amino acids such as glutamine, glutamate, aspartate, and asparagine are conserved between strains. Finally, we generated mutants lacking the quorum-sensing-dependent regulator PhcA in four diverse strains, and we showed that the phcA-dependent trade-off between growth and production of virulence factors is conserved across the R. solanacearum species complex. IMPORTANCE: Ralstonia solanacearum is one of the most important threats to plant health worldwide, causing disease on a very large range of agricultural crops such as tomato or potato. Behind the R. solanacearum name are hundreds of strains with different host range and lifestyle, classified into three species. Studying the differences between strains allows to better apprehend the biology of the pathogens and the specificity of some strains. None of the published genomic comparative studies have focused on the metabolism of the strains so far. We developed a new bioinformatic pipeline to build high-quality metabolic networks and used a combination of metabolic modeling and high-throughput phenotypic Biolog microplates to look for the metabolic differences between 11 strains across the three species. Our study revealed that genes encoding enzymes are overall conserved, with few variations between strains. However, more variations were observed when considering substrate usage. These variations probably result from regulation rather than the presence or absence of enzymes in the genome. American Society for Microbiology 2023-06-21 /pmc/articles/PMC10470067/ /pubmed/37341493 http://dx.doi.org/10.1128/msystems.00083-23 Text en Copyright © 2023 Baroukh et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Baroukh, Caroline
Cottret, Ludovic
Pires, Emma
Peyraud, Rémi
Guidot, Alice
Genin, Stéphane
Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title_full Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title_fullStr Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title_full_unstemmed Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title_short Insights into the metabolic specificities of pathogenic strains from the Ralstonia solanacearum species complex
title_sort insights into the metabolic specificities of pathogenic strains from the ralstonia solanacearum species complex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470067/
https://www.ncbi.nlm.nih.gov/pubmed/37341493
http://dx.doi.org/10.1128/msystems.00083-23
work_keys_str_mv AT baroukhcaroline insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex
AT cottretludovic insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex
AT piresemma insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex
AT peyraudremi insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex
AT guidotalice insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex
AT geninstephane insightsintothemetabolicspecificitiesofpathogenicstrainsfromtheralstoniasolanacearumspeciescomplex