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Chemical warfare between leafcutter ant symbionts and a co-evolved pathogen

Author

Listed:
  • Daniel Heine

    (John Innes Centre)

  • Neil A. Holmes

    (University of East Anglia)

  • Sarah F. Worsley

    (University of East Anglia)

  • Ana Carolina A. Santos

    (HKI
    Friedrich Schiller University
    Universidade Federal de São Carlos, UFSCar)

  • Tabitha M. Innocent

    (University of Copenhagen)

  • Kirstin Scherlach

    (HKI)

  • Elaine H. Patrick

    (University of East Anglia)

  • Douglas W. Yu

    (University of East Anglia)

  • J. Colin Murrell

    (University of East Anglia)

  • Paulo C. Vieria

    (Universidade Federal de São Carlos, UFSCar)

  • Jacobus J. Boomsma

    (University of Copenhagen)

  • Christian Hertweck

    (HKI
    Friedrich Schiller University)

  • Matthew I. Hutchings

    (University of East Anglia)

  • Barrie Wilkinson

    (John Innes Centre)

Abstract

Acromyrmex leafcutter ants form a mutually beneficial symbiosis with the fungus Leucoagaricus gongylophorus and with Pseudonocardia bacteria. Both are vertically transmitted and actively maintained by the ants. The fungus garden is manured with freshly cut leaves and provides the sole food for the ant larvae, while Pseudonocardia cultures are reared on the ant-cuticle and make antifungal metabolites to help protect the cultivar against disease. If left unchecked, specialized parasitic Escovopsis fungi can overrun the fungus garden and lead to colony collapse. We report that Escovopsis upregulates the production of two specialized metabolites when it infects the cultivar. These compounds inhibit Pseudonocardia and one, shearinine D, also reduces worker behavioral defenses and is ultimately lethal when it accumulates in ant tissues. Our results are consistent with an active evolutionary arms race between Pseudonocardia and Escovopsis, which modifies both bacterial and behavioral defenses such that colony collapse is unavoidable once Escovopsis infections escalate.

Suggested Citation

  • Daniel Heine & Neil A. Holmes & Sarah F. Worsley & Ana Carolina A. Santos & Tabitha M. Innocent & Kirstin Scherlach & Elaine H. Patrick & Douglas W. Yu & J. Colin Murrell & Paulo C. Vieria & Jacobus J, 2018. "Chemical warfare between leafcutter ant symbionts and a co-evolved pathogen," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04520-1
    DOI: 10.1038/s41467-018-04520-1
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    Cited by:

    1. Elena Seibel & Soohyun Um & Kasun H. Bodawatta & Anna J. Komor & Tanya Decker & Janis Fricke & Robert Murphy & Gibson Maiah & Bulisa Iova & Hannah Maus & Tanja Schirmeister & Knud Andreas Jønsson & Mi, 2024. "Bacteria from the Amycolatopsis genus associated with a toxic bird secrete protective secondary metabolites," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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