Abstract

Agricultural soil harbors a diverse microbiome that can form beneficial relationships with plants, including the inhibition of plant pathogens. Pseudomonas spp. are one of the most abundant bacterial genera in the soil and rhizosphere and play important roles in promoting plant health. However, the genetic determinants of this beneficial activity are only partially understood. Here, we genetically and phenotypically characterize the Pseudomonas fluorescens population in a commercial potato field, where we identify strong correlations between specialized metabolite biosynthesis and antagonism of the potato pathogens Streptomyces scabies and Phytophthora infestans. Genetic and chemical analyses identified hydrogen cyanide and cyclic lipopeptides as key specialized metabolites associated with S. scabies inhibition, which was supported by in planta biocontrol experiments. We show that a single potato field contains a hugely diverse and dynamic population of Pseudomonas bacteria, whose capacity to produce specialized metabolites is shaped both by plant colonization and defined environmental inputs.

Data availability

Genome assemblies are available at the European Nucleotide Archive (http://www.ebi.ac.uk/ena/) with the project accession PRJEB34261.Mass spectrometry data are available as a MassIVE dataset at ftp://massive.ucsd.edu/MSV000084283/ and the GNPS analysis is available here:https://gnps.ucsd.edu/ProteoSAFe/status.jsp?task=51ac5fe596424cf88cfc17898985cac2All other data generated in this study are included in the manuscript and supporting files.

The following data sets were generated

Article and author information

Author details

  1. Alba Pacheco-Moreno

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  2. Francesca L Stefanato

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  3. Jonathan J Ford

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9886-690X
  4. Christine Trippel

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  5. Simon Uszkoreit

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  6. Laura Ferrafiat

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  7. Lucia Grenga

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  8. Ruth Dickens

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  9. Nathan Kelly

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  10. Alexander DH Kingdon

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7074-6893
  11. Liana Ambrosetti

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  12. Sergey A Nepogodiev

    Department of Biochemistry and Metabolism, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9796-4612
  13. Kim C Findlay

    Department of Cell and Developmental Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  14. Jitender Cheema

    Department of Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  15. Martin Trick

    Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  16. Govind Chandra

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7882-6676
  17. Graham Tomalin

    VCS Potatoes, Framlingham, United Kingdom
    Competing interests
    Graham Tomalin, Graham Tomalin is affiliated with VCS Potatoes. The author has no financial interests to declare..
  18. Jacob G Malone

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    jacob.malone@jic.ac.uk
    Competing interests
    No competing interests declared.
  19. Andrew W Truman

    Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    andrew.truman@jic.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5453-7485

Funding

Biotechnology and Biological Sciences Research Council (BB/J004596/1)

  • Andrew W Truman

Biotechnology and Biological Sciences Research Council (BBS/E/J/000PR9790)

  • Andrew W Truman

Biotechnology and Biological Sciences Research Council (BB/J004553/1)

  • Jacob G Malone

Biotechnology and Biological Sciences Research Council (BBS/E/J/000PR9797)

  • Jacob G Malone

Biotechnology and Biological Sciences Research Council (BB/M011216/1)

  • Alba Pacheco-Moreno
  • Jonathan J Ford

NPRONET (POC021)

  • Graham Tomalin
  • Jacob G Malone
  • Andrew W Truman

Royal Society (URF\R\180007)

  • Andrew W Truman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. María Mercedes Zambrano, CorpoGen, Colombia

Version history

  1. Preprint posted: September 26, 2019 (view preprint)
  2. Received: July 2, 2021
  3. Accepted: November 16, 2021
  4. Accepted Manuscript published: November 18, 2021 (version 1)
  5. Version of Record published: December 31, 2021 (version 2)

Copyright

© 2021, Pacheco-Moreno et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alba Pacheco-Moreno
  2. Francesca L Stefanato
  3. Jonathan J Ford
  4. Christine Trippel
  5. Simon Uszkoreit
  6. Laura Ferrafiat
  7. Lucia Grenga
  8. Ruth Dickens
  9. Nathan Kelly
  10. Alexander DH Kingdon
  11. Liana Ambrosetti
  12. Sergey A Nepogodiev
  13. Kim C Findlay
  14. Jitender Cheema
  15. Martin Trick
  16. Govind Chandra
  17. Graham Tomalin
  18. Jacob G Malone
  19. Andrew W Truman
(2021)
Pan-genome analysis identifies intersecting roles for Pseudomonas specialized metabolites in potato pathogen inhibition
eLife 10:e71900.
https://doi.org/10.7554/eLife.71900

Share this article

https://doi.org/10.7554/eLife.71900

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