The xylan utilization system of the plant pathogen Xanthomonas campestris pv campestris controls epiphytic life and reveals common features with oligotrophic bacteria and animal gut symbionts

Authors

  • Guillaume Déjean,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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    • These authors contributed equally to this work.
  • Servane Blanvillain-Baufumé,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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    • These authors contributed equally to this work.
  • Alice Boulanger,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Armelle Darrasse,

    1. INRA, UMR 1345, Institut de Recherche en Horticulture et Semences (IRHS), Beaucouzé CEDEX 01, France
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  • Thomas Dugé de Bernonville,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Anne-Laure Girard,

    1. INRA, UMR 1345, Institut de Recherche en Horticulture et Semences (IRHS), Beaucouzé CEDEX 01, France
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  • Sébastien Carrére,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Stevie Jamet,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Claudine Zischek,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Martine Lautier,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
    3. Université de Toulouse, Université Paul Sabatier, Toulouse, France
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  • Magali Solé,

    1. Institut für Biologie, Bereich Genetik, Martin-Luther-Universität Halle-Wittenberg, Halle (Saale), Germany
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  • Daniela Büttner,

    1. Institut für Biologie, Bereich Genetik, Martin-Luther-Universität Halle-Wittenberg, Halle (Saale), Germany
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  • Marie-Agnès Jacques,

    1. INRA, UMR 1345, Institut de Recherche en Horticulture et Semences (IRHS), Beaucouzé CEDEX 01, France
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  • Emmanuelle Lauber,

    1. INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
    2. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
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  • Matthieu Arlat

    Corresponding author
    1. CNRS, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France
    2. Université de Toulouse, Université Paul Sabatier, Toulouse, France
    • INRA, Laboratoire des Interactions Plantes–Microorganismes (LIPM), UMR441, Castanet-Tolosan, France
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Author for correspondence:

Matthieu Arlat

Tel: +33 561 285 047

Email: matthieu.arlat@toulouse.inra.fr

Summary

  • Xylan is a major structural component of plant cell wall and the second most abundant plant polysaccharide in nature.
  • Here, by combining genomic and functional analyses, we provide a comprehensive picture of xylan utilization by Xanthomonas campestris pv campestris (Xcc) and highlight its role in the adaptation of this epiphytic phytopathogen to the phyllosphere.
  • The xylanolytic activity of Xcc depends on xylan-deconstruction enzymes but also on transporters, including two TonB-dependent outer membrane transporters (TBDTs) which belong to operons necessary for efficient growth in the presence of xylo-oligosaccharides and for optimal survival on plant leaves. Genes of this xylan utilization system are specifically induced by xylo-oligosaccharides and repressed by a LacI-family regulator named XylR.
  • Part of the xylanolytic machinery of Xcc, including TBDT genes, displays a high degree of conservation with the xylose-regulon of the oligotrophic aquatic bacterium Caulobacter crescentus. Moreover, it shares common features, including the presence of TBDTs, with the xylan utilization systems of Bacteroides ovatus and Prevotella bryantii, two gut symbionts. These similarities and our results support an important role for TBDTs and xylan utilization systems for bacterial adaptation in the phyllosphere, oligotrophic environments and animal guts.

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