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Spatial analysis of the root system coupled to microbial community inoculation shed light on rhizosphere bacterial community assembly

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Abstract

Although studied for more than a century, the spatial distribution of microorganisms in a root system still remains partly understood. In a repeated greenhouse experiment using the model plant Brachypodium distachyon, we investigated the composition and distribution of rhizosphere bacteria and their response to inoculation with artificially selected microbial communities, using two different sampling scales: root sections from distinct individual roots (apical, middle, and rear sections) and the remaining entire system recovered after homogenization. Using 16S rRNA gene sequencing, we identified that root section identity was the most influential factor on the microbiota composition (R2 = 44.4%), followed by batch (R2 = 34.4%), and plant identity (R2 = 15.2%). Apical sections were characterized by increased abundances for Firmicutes members, while the rear sections featured more Verrucomicrobia. Root section sampling showed better sensitivity at detecting significant effects of the inoculation on the microbiota composition (e.g., local influence of inoculation on rear sections), in contrast, the homogenized sampling showed improved reproducibility (e.g., smaller sample dispersion). The comparison of the two sampling strategies highlighted a clear tradeoff between reproducibility and sensitivity, encouraging to complement traditional approaches with fine-scale sampling to improve our capacity to understand biological effects that could be otherwise missed.

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Data availability

The data that support the findings of this study are openly available in the Sequence Read Archive (SRA) repository at https://www.ncbi.nlm.nih.gov/bioproject/PRJNA635875.

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The code is available from the corresponding author upon request.

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Acknowledgements

We thank the Lundbeck Foundation (grant number R223-2016-179) for funding this study. S.W. was supported by the China Scholarship Council. S.J. was supported by the University of Bourgogne Franche-Comté via the FABER program (grant number 2017-9201AAO049S01302) and via the ISITE-BFC International Junior Fellowship award (AAP3: RA19028.AEC.IS). We express our gratitude to the members of the 4PMI platform lead by Christophe Salon and Céline Bernard for their expertise and help during plant phenotyping (For Plant and Microbe Interaction, INRA Center Dijon, France, https://www6.dijon.inrae.fr/plateforme4pmi_eng/Technical-description/High-Throughput-phenotyping). Respectively, we thank Damien Gironde, Frédéric Saignole, Noureddine El-Mjiyad and Karine Palavioux for helping during plant growth monitoring; Franck Zenk and Julien Martinet for image capture; and Mickael Lamboeuf for image processing; Sébastien Anselme, Richard Sibout, and Thomas Girin from the Brachypodium resources center at the Institut Jean Pierre-Bourgin, (INRAVersailles, France) for seeds provision; Beatriz Decencière, Amandine Hansart, and Florent Massol of the CEREEP—Ecotron IDF/UMS CNRS/ENS 3194 for soil provision.

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S.J.S., M.B., and L.P. designed the study. S.W. and S.J. carried out the study. S.W., S.J., M.B. contributed to the statistical analysis. M.B., S.J., S.J.S., L.P., and S.W. contributed to the concept and interpretation of the data. S.W. wrote the manuscript and S.J. made a substantial contribution to the revision of the manuscript.

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Correspondence to Søren Johannes Sørensen.

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The authors declare no conflict of interest.

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Shaodong Wei and Samuel Jacquiod Shared first author contributions.

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Wei, S., Jacquiod, S., Philippot, L. et al. Spatial analysis of the root system coupled to microbial community inoculation shed light on rhizosphere bacterial community assembly. Biol Fertil Soils 57, 973–989 (2021). https://doi.org/10.1007/s00374-021-01590-0

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  • DOI: https://doi.org/10.1007/s00374-021-01590-0

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