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Genome-resolved metatranscriptomics reveals conserved root colonization determinants in a synthetic microbiota

Author

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  • Nathan Vannier

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research
    IGEPP, INRAE, Institut Agro, Univ Rennes)

  • Fantin Mesny

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research
    University of Cologne)

  • Felix Getzke

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research)

  • Guillaume Chesneau

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research)

  • Laura Dethier

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research)

  • Jana Ordon

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research)

  • Thorsten Thiergart

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research)

  • Stéphane Hacquard

    (Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research
    Cluster of Excellence on Plant Sciences, Max Planck Institute for Plant Breeding Research)

Abstract

The identification of processes activated by specific microbes during microbiota colonization of plant roots has been hampered by technical constraints in metatranscriptomics. These include lack of reference genomes, high representation of host or microbial rRNA sequences in datasets, or difficulty to experimentally validate gene functions. Here, we recolonized germ-free Arabidopsis thaliana with a synthetic, yet representative root microbiota comprising 106 genome-sequenced bacterial and fungal isolates. We used multi-kingdom rRNA depletion, deep RNA-sequencing and read mapping against reference microbial genomes to analyse the in planta metatranscriptome of abundant colonizers. We identified over 3,000 microbial genes that were differentially regulated at the soil-root interface. Translation and energy production processes were consistently activated in planta, and their induction correlated with bacterial strains’ abundance in roots. Finally, we used targeted mutagenesis to show that several genes consistently induced by multiple bacteria are required for root colonization in one of the abundant bacterial strains (a genetically tractable Rhodanobacter). Our results indicate that microbiota members activate strain-specific processes but also common gene sets to colonize plant roots.

Suggested Citation

  • Nathan Vannier & Fantin Mesny & Felix Getzke & Guillaume Chesneau & Laura Dethier & Jana Ordon & Thorsten Thiergart & Stéphane Hacquard, 2023. "Genome-resolved metatranscriptomics reveals conserved root colonization determinants in a synthetic microbiota," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43688-z
    DOI: 10.1038/s41467-023-43688-z
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    References listed on IDEAS

    as
    1. Fantin Mesny & Shingo Miyauchi & Thorsten Thiergart & Brigitte Pickel & Lea Atanasova & Magnus Karlsson & Bruno Hüttel & Kerrie W. Barry & Sajeet Haridas & Cindy Chen & Diane Bauer & William Andreopou, 2021. "Genetic determinants of endophytism in the Arabidopsis root mycobiome," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    3. Gabriel Castrillo & Paulo José Pereira Lima Teixeira & Sur Herrera Paredes & Theresa F. Law & Laura de Lorenzo & Meghan E. Feltcher & Omri M. Finkel & Natalie W. Breakfield & Piotr Mieczkowski & Corbi, 2017. "Root microbiota drive direct integration of phosphate stress and immunity," Nature, Nature, vol. 543(7646), pages 513-518, March.
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