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

Nathan Vannier, Fantin Mesny, Felix Getzke, Guillaume Chesneau, Laura Dethier, Jana Ordon, Thorsten Thiergart and Stéphane Hacquard ()
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Nathan Vannier: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research
Fantin Mesny: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research
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

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-43688-z

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