Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts

Abstract The emergence of commensalism and mutualism often derives from ancestral parasitism. However, in the case of rhizobium-legume interactions, bacterial strains displaying both pathogenic and nodulation features on a single host have not been described yet. Here, we isolated such a bacterium f...

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Main Authors: Kévin Magne, Sophie Massot, Tifaine Folletti, Laurent Sauviac, Elhosseyn Ait-Salem, Ilona Pires, Maged M. Saad, Abdul Aziz Eida, Salim Bougouffa, Adrien Jugan, Eleonora Rolli, Raphaël Forquet, Virginie Puech-Pages, Fabienne Maillet, Gautier Bernal, Chrystel Gibelin, Heribert Hirt, Véronique Gruber, Rémi Peyraud, Fabienne Vailleau, Benjamin Gourion, Pascal Ratet
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-53388-x
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author Kévin Magne
Sophie Massot
Tifaine Folletti
Laurent Sauviac
Elhosseyn Ait-Salem
Ilona Pires
Maged M. Saad
Abdul Aziz Eida
Salim Bougouffa
Adrien Jugan
Eleonora Rolli
Raphaël Forquet
Virginie Puech-Pages
Fabienne Maillet
Gautier Bernal
Chrystel Gibelin
Heribert Hirt
Véronique Gruber
Rémi Peyraud
Fabienne Vailleau
Benjamin Gourion
Pascal Ratet
author_facet Kévin Magne
Sophie Massot
Tifaine Folletti
Laurent Sauviac
Elhosseyn Ait-Salem
Ilona Pires
Maged M. Saad
Abdul Aziz Eida
Salim Bougouffa
Adrien Jugan
Eleonora Rolli
Raphaël Forquet
Virginie Puech-Pages
Fabienne Maillet
Gautier Bernal
Chrystel Gibelin
Heribert Hirt
Véronique Gruber
Rémi Peyraud
Fabienne Vailleau
Benjamin Gourion
Pascal Ratet
author_sort Kévin Magne
collection DOAJ
description Abstract The emergence of commensalism and mutualism often derives from ancestral parasitism. However, in the case of rhizobium-legume interactions, bacterial strains displaying both pathogenic and nodulation features on a single host have not been described yet. Here, we isolated such a bacterium from Medicago nodules. On the same plant genotypes, the T4 strain can induce ineffective nodules in a highly competitive way and behave as a harsh parasite triggering plant death. The T4 strain presents this dual ability on multiple legume species of the Inverted Repeat-Lacking Clade, the output of the interaction relying on the developmental stage of the plant. Genomic and phenotypic clustering analysis show that T4 belongs to the nonsymbiotic Ensifer adhaerens group and clusters together with T173, another strain harboring this dual ability. In this work, we identify a bacterial clade that includes rhizobial strains displaying both pathogenic and nodulating abilities on a single legume host.
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spelling doaj-art-672ba4366b3048039d80fa88f3a2cf352025-08-20T02:11:28ZengNature PortfolioNature Communications2041-17232024-10-0115111310.1038/s41467-024-53388-xAtypical rhizobia trigger nodulation and pathogenesis on the same legume hostsKévin Magne0Sophie Massot1Tifaine Folletti2Laurent Sauviac3Elhosseyn Ait-Salem4Ilona Pires5Maged M. Saad6Abdul Aziz Eida7Salim Bougouffa8Adrien Jugan9Eleonora Rolli10Raphaël Forquet11Virginie Puech-Pages12Fabienne Maillet13Gautier Bernal14Chrystel Gibelin15Heribert Hirt16Véronique Gruber17Rémi Peyraud18Fabienne Vailleau19Benjamin Gourion20Pascal Ratet21Université Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayDARWIN21, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and TechnologyDARWIN21, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and TechnologyComputational Bioscience Research Center, King Abdullah University of Science and TechnologyUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayiMEANLaboratoire de Recherche en Sciences Végétales, CNRS, UPS, Toulouse INP, Université de ToulouseLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSDARWIN21, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and TechnologyUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayiMEANLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSLaboratoire des Interactions Plantes Microbes Environnement, Université de Toulouse, INRAE, CNRSUniversité Paris-Saclay, CNRS, INRAE, Université Evry, Institute of Plant Sciences Paris-SaclayAbstract The emergence of commensalism and mutualism often derives from ancestral parasitism. However, in the case of rhizobium-legume interactions, bacterial strains displaying both pathogenic and nodulation features on a single host have not been described yet. Here, we isolated such a bacterium from Medicago nodules. On the same plant genotypes, the T4 strain can induce ineffective nodules in a highly competitive way and behave as a harsh parasite triggering plant death. The T4 strain presents this dual ability on multiple legume species of the Inverted Repeat-Lacking Clade, the output of the interaction relying on the developmental stage of the plant. Genomic and phenotypic clustering analysis show that T4 belongs to the nonsymbiotic Ensifer adhaerens group and clusters together with T173, another strain harboring this dual ability. In this work, we identify a bacterial clade that includes rhizobial strains displaying both pathogenic and nodulating abilities on a single legume host.https://doi.org/10.1038/s41467-024-53388-x
spellingShingle Kévin Magne
Sophie Massot
Tifaine Folletti
Laurent Sauviac
Elhosseyn Ait-Salem
Ilona Pires
Maged M. Saad
Abdul Aziz Eida
Salim Bougouffa
Adrien Jugan
Eleonora Rolli
Raphaël Forquet
Virginie Puech-Pages
Fabienne Maillet
Gautier Bernal
Chrystel Gibelin
Heribert Hirt
Véronique Gruber
Rémi Peyraud
Fabienne Vailleau
Benjamin Gourion
Pascal Ratet
Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
Nature Communications
title Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
title_full Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
title_fullStr Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
title_full_unstemmed Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
title_short Atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
title_sort atypical rhizobia trigger nodulation and pathogenesis on the same legume hosts
url https://doi.org/10.1038/s41467-024-53388-x
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