Chromatin mapping identifies BasR, a key regulator of bacteria-triggered production of fungal secondary metabolites

  1. Juliane Fischer
  2. Sebastian Y Müller
  3. Tina Netzker
  4. Nils Jäger
  5. Agnieszka Gacek-Matthews
  6. Kirstin Scherlach
  7. Maria C Stroe
  8. María García-Altares
  9. Francesco Pezzini
  10. Hanno Schoeler
  11. Michael Reichelt
  12. Jonathan Gershenzon
  13. Mario KC Krespach
  14. Ekaterina Shelest
  15. Volker Schroeckh
  16. Vito Valiante
  17. Thorsten Heinzel
  18. Christian Hertweck
  19. Joseph Strauss  Is a corresponding author
  20. Axel A Brakhage  Is a corresponding author
  1. Leibniz Institute for Natural Product Research and Infection Biology (HKI), Germany
  2. Hans Knöll Institute, Germany
  3. Friedrich Schiller University Jena, Germany
  4. BOKU-University of Natural Resources and Life Sciences, Austria
  5. Max Planck Institute for Chemical Ecology, Germany

Abstract

The eukaryotic epigenetic machinery can be modified by bacteria to reprogram the response of eukaryotes during their interaction with microorganisms. We discovered that the bacterium Streptomyces rapamycinicus triggered increased chromatin acetylation and thus activation of the silent secondary metabolism ors gene cluster in the fungus Aspergillus nidulans. Using this model we aim at understanding mechanisms of microbial communication based on bacteria-triggered chromatin modification. By genome-wide ChIP-seq analysis of acetylated histone H3 we uncovered the unique chromatin landscape in A. nidulans upon co-cultivation with S. rapamycinicus and relate changes in the acetylation to that in the fungal transcriptome. Differentially acetylated histones were detected in genes involved in secondary metabolism, amino acid and nitrogen metabolism, signaling, and encoding transcription factors. Further molecular analyses identified the Myb-like transcription factor BasR as the regulatory node for transduction of the bacterial signal in the fungus and show its function is conserved in other Aspergillus species.

Data availability

ChIP-seq data were deposited in the ArrayExpress database at EMBL-EBI (www.ebi.ac.uk/arrayexpress) under accession number E-MTAB-5819.

The following data sets were generated

Article and author information

Author details

  1. Juliane Fischer

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    Competing interests
    No competing interests declared.
  2. Sebastian Y Müller

    Systems Biology and Bioinformatics, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  3. Tina Netzker

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    Competing interests
    No competing interests declared.
  4. Nils Jäger

    Department of Biochemistry, Friedrich Schiller University Jena, Jena, Germany
    Competing interests
    No competing interests declared.
  5. Agnieszka Gacek-Matthews

    Department for Applied Genetics and Cell Biology, BOKU-University of Natural Resources and Life Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  6. Kirstin Scherlach

    Department of Biomolecular Chemistry, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  7. Maria C Stroe

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    Competing interests
    No competing interests declared.
  8. María García-Altares

    Department of Biomolecular Chemistry, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  9. Francesco Pezzini

    Systems Biology and Bioinformatics, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  10. Hanno Schoeler

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    Competing interests
    No competing interests declared.
  11. Michael Reichelt

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  12. Jonathan Gershenzon

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  13. Mario KC Krespach

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    Competing interests
    No competing interests declared.
  14. Ekaterina Shelest

    Systems Biology and Bioinformatics, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  15. Volker Schroeckh

    Department of Molecular and Applied Microbiology, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  16. Vito Valiante

    Leibniz Research Group - Biobricks of Microbial Natural Product Syntheses, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  17. Thorsten Heinzel

    Department of Biochemistry, Friedrich Schiller University Jena, Jena, Germany
    Competing interests
    No competing interests declared.
  18. Christian Hertweck

    Department of Biomolecular Chemistry, Hans Knöll Institute, Jena, Germany
    Competing interests
    No competing interests declared.
  19. Joseph Strauss

    Department for Applied Genetics and Cell Biology, BOKU-University of Natural Resources and Life Sciences, Vienna, Austria
    For correspondence
    joseph.strauss@boku.ac.at
    Competing interests
    No competing interests declared.
  20. Axel A Brakhage

    Department of Molecular and Applied Microbiology, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena, Germany
    For correspondence
    axel.brakhage@hki-jena.de
    Competing interests
    Axel A Brakhage, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8814-4193

Funding

Deutsche Forschungsgemeinschaft (SFB 1127)

  • Tina Netzker
  • Nils Jäger
  • Ekaterina Shelest

Bundesministerium für Bildung und Forschung (InfectControl2020)

  • Maria C Stroe

Horizon 2020 Framework Programme (IF-EF; Project reference 700036)

  • María García-Altares

Leibniz-Gemeinschaft

  • Juliane Fischer

Deutsche Forschungsgemeinschaft (GSC 214)

  • Mario KC Krespach

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

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Version history

  1. Received: August 10, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 12, 2018 (version 1)
  4. Version of Record published: November 13, 2018 (version 2)

Copyright

© 2018, Fischer 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. Juliane Fischer
  2. Sebastian Y Müller
  3. Tina Netzker
  4. Nils Jäger
  5. Agnieszka Gacek-Matthews
  6. Kirstin Scherlach
  7. Maria C Stroe
  8. María García-Altares
  9. Francesco Pezzini
  10. Hanno Schoeler
  11. Michael Reichelt
  12. Jonathan Gershenzon
  13. Mario KC Krespach
  14. Ekaterina Shelest
  15. Volker Schroeckh
  16. Vito Valiante
  17. Thorsten Heinzel
  18. Christian Hertweck
  19. Joseph Strauss
  20. Axel A Brakhage
(2018)
Chromatin mapping identifies BasR, a key regulator of bacteria-triggered production of fungal secondary metabolites
eLife 7:e40969.
https://doi.org/10.7554/eLife.40969

Share this article

https://doi.org/10.7554/eLife.40969

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