Article

Functional overlap of the Arabidopsis leaf and root microbiota

  • Nature volume 528, pages 364369 (17 December 2015)
  • doi:10.1038/nature16192
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Abstract

Roots and leaves of healthy plants host taxonomically structured bacterial assemblies, and members of these communities contribute to plant growth and health. We established Arabidopsis leaf- and root-derived microbiota culture collections representing the majority of bacterial species that are reproducibly detectable by culture-independent community sequencing. We found an extensive taxonomic overlap between the leaf and root microbiota. Genome drafts of 400 isolates revealed a large overlap of genome-encoded functional capabilities between leaf- and root-derived bacteria with few significant differences at the level of individual functional categories. Using defined bacterial communities and a gnotobiotic Arabidopsis plant system we show that the isolates form assemblies resembling natural microbiota on their cognate host organs, but are also capable of ectopic leaf or root colonization. While this raises the possibility of reciprocal relocation between root and leaf microbiota members, genome information and recolonization experiments also provide evidence for microbiota specialization to their respective niche.

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Accessions

Primary accessions

European Nucleotide Archive

Data deposits

Sequencing reads (454 16S rRNA, MiSeq 16S rRNA and WGS HiSeq reads) have been deposited in the European Nucleotide Archive (ENA) under accession numbers PRJEB11545, PRJEB11583 and PRJEB11584, and genome assemblies and annotations corresponding to the leaf, root and soil culture collections have been deposited in the BioProject database under accession numbers PRJNA297956, PRJNA297942 and PRJNA298127. Isolates have been deposited at the Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures (https://www.dsmz.de/).

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Acknowledgements

We thank D. Lundberg, S. Lebeis, S. Herrera-Paredes, S. Biswas and J. Dangl for sharing the calcined clay utilization protocol before publication; M. Kisielow of the ETH Zurich Flow Cytometry Core Facility for help with bacterial cell sorting as well as M. Baltisberger, D. Jolic and D. Weigel for their help in finding natural Arabidopsis populations; E. Kemen and M. Agler for sharing the Illumina Mi-Seq protocol for profiling of defined communities before publication and A. Sczyrba for his advice with the genome assembly. This work was supported by funds to P.S.-L. from the Max Planck Society, a European Research Council advanced grant (ROOTMICROBIOTA), the ‘Cluster of Excellence on Plant Sciences’ program funded by the Deutsche Forschungsgemeinschaft, the German Center for Infection Research (DZIF), by funds to J.A.V. from ETH Zurich (ETH Research Grant ETH-41 14-2), a grant from the Swiss National Research Foundation (310030B_152835), and a European Research Council advanced grant (PhyMo).

Author information

Author notes

    • Yang Bai
    • , Daniel B. Müller
    • , Girish Srinivas
    • , Ruben Garrido-Oter
    • , Julia A. Vorholt
    •  & Paul Schulze-Lefert

    These authors contributed equally to this work.

Affiliations

  1. Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany

    • Yang Bai
    • , Girish Srinivas
    • , Ruben Garrido-Oter
    • , Matthias Rott
    • , Nina Dombrowski
    • , Stijn Spaepen
    •  & Paul Schulze-Lefert
  2. Institute of Microbiology, ETH Zurich, 8093 Zurich, Switzerland

    • Daniel B. Müller
    • , Eva Potthoff
    • , Mitja Remus-Emsermann
    •  & Julia A. Vorholt
  3. Department of Algorithmic Bioinformatics, Heinrich Heine University Düsseldorf, 40225 Düsseldorf, Germany

    • Ruben Garrido-Oter
  4. Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany

    • Ruben Garrido-Oter
    • , Alice C. McHardy
    •  & Paul Schulze-Lefert
  5. Computational Biology of Infection Research, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany

    • Philipp C. Münch
    •  & Alice C. McHardy
  6. Max-von-Pettenkofer Institute, Ludwig Maximilian University, German Center for Infection Research (DZIF), partner site LMU Munich, 80336 Munich, Germany

    • Philipp C. Münch
  7. German Center for Infection Research (DZIF), partner site Hannover-Braunschweig, 38124 Braunschweig, Germany

    • Philipp C. Münch
  8. Max Planck Genome Center, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany

    • Bruno Hüttel

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Contributions

J.A.V. and P.S.-L. initiated, coordinated and supervised the project. Y.B., M.R., N.D. and S.S. isolated root and soil bacteria strains. Y.B. collected root material and performed culture-independent community profiling. D.B.M., E.P. and M.R.-E. collected environmental leaf material, D.B.M. and E.P. isolated leaf strains and performed culture-independent community profiling. G.S. and R.G.-O. analysed culture-independent 16S rRNA amplicon sequencing data. Y.B., D.B.M. isolated DNA and prepared samples for genome sequencing. R.G.-O., P.C.M, B.H. and A.C.M. organized the genome sequencing data. R.G.-O. assembled and annotated draft genomes and performed comparative genome analyses. Y.B. and D.B.M. performed recolonization experiments; G.S. and R.G.-O. analysed the recolonization data. Y.B., D.B.M., R.G.-O., J.A.V. and P.S.-L. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Julia A. Vorholt or Paul Schulze-Lefert.

Extended data

Supplementary information

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    Supplementary Data

    This zipped folder contains Supplementary Data files 1-7 and a Supplementary Data guide.

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