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T6SS contributes to gut microbiome invasion and killing of an herbivorous pest insect by plant-beneficial Pseudomonas protegens

The ISME Journal (2019) | Download Citation

Abstract

Pseudomonas protegens are multi-talented plant-colonizing bacteria that suppress plant pathogens and stimulate plant defenses. In addition, they are capable of invading and killing agriculturally important plant pest insects that makes them promising candidates for biocontrol applications. Here we assessed the role of type VI secretion system (T6SS) components of type strain CHA0 during interaction with larvae of the cabbage pest Pieris brassicae. We show that the T6SS core apparatus and two VgrG modules, encompassing the respective T6SS spikes (VgrG1a and VgrG1b) and associated effectors (RhsA and Ghh1), contribute significantly to insect pathogenicity of P. protegens in oral infection assays but not when bacteria are injected directly into the hemolymph. Monitoring of the colonization levels of P. protegens in the gut, hemolymph, and excrements of the insect larvae revealed that the invader relies on T6SS and VgrG1a module function to promote hemocoel invasion. A 16S metagenomic analysis demonstrated that T6SS-supported invasion by P. protegens induces significant changes in the insect gut microbiome affecting notably Enterobacteriaceae, a dominant group of the commensal gut bacteria. Our study supports the concept that pathogens deploy T6SS-based strategies to disrupt the commensal microbiota in order to promote host colonization and pathogenesis.

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Acknowledgements

We gratefully acknowledge the group of Philippe Reymond at the Department of Plant Molecular Biology of the University of Lausanne for help with rearing Pieris brassicae and with the development of the artificial diet-based feeding assay. We thank the Biocommunications group (Consuelo De Moraes), Department of Environmental System Science, ETH Zurich for providing eggs of Pieris brassicae.

Sources of support (grants/equipment)

This study was supported by grant 31003A-159520 from the Swiss National Foundation for Scientific Research.

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Affiliations

  1. Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland

    • Jordan Vacheron
    • , Maria Péchy-Tarr
    • , Silvia Brochet
    • , Clara Margot Heiman
    • , Marina Stojiljkovic
    •  & Christoph Keel
  2. Plant Pathology, Institute of Integrative Biology, Swiss Federal Institute of Technology (ETH) Zurich, Zurich, Switzerland

    • Monika Maurhofer

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The authors declare that they have no conflict of interest.

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Correspondence to Monika Maurhofer or Christoph Keel.

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https://doi.org/10.1038/s41396-019-0353-8