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Streptomyces umbrella toxin particles block hyphal growth of competing species

Author

Listed:
  • Qinqin Zhao

    (University of Washington)

  • Savannah Bertolli

    (University of Washington)

  • Young-Jun Park

    (University of Washington
    University of Washington)

  • Yongjun Tan

    (St Louis University)

  • Kevin J. Cutler

    (University of Washington
    University of Washington)

  • Pooja Srinivas

    (University of Washington)

  • Kyle L. Asfahl

    (University of Washington
    University of Washington)

  • Citlali Fonesca-García

    (USDA-ARS
    University of California Berkeley)

  • Larry A. Gallagher

    (University of Washington)

  • Yaqiao Li

    (University of Washington)

  • Yaxi Wang

    (University of Washington)

  • Devin Coleman-Derr

    (USDA-ARS
    University of California Berkeley)

  • Frank DiMaio

    (University of Washington
    University of Washington)

  • Dapeng Zhang

    (St Louis University
    St Louis University)

  • S. Brook Peterson

    (University of Washington)

  • David Veesler

    (University of Washington
    University of Washington)

  • Joseph D. Mougous

    (University of Washington
    University of Washington
    University of Washington)

Abstract

Streptomyces are a genus of ubiquitous soil bacteria from which the majority of clinically utilized antibiotics derive1. The production of these antibacterial molecules reflects the relentless competition Streptomyces engage in with other bacteria, including other Streptomyces species1,2. Here we show that in addition to small-molecule antibiotics, Streptomyces produce and secrete antibacterial protein complexes that feature a large, degenerate repeat-containing polymorphic toxin protein. A cryo-electron microscopy structure of these particles reveals an extended stalk topped by a ringed crown comprising the toxin repeats scaffolding five lectin-tipped spokes, which led us to name them umbrella particles. Streptomyces coelicolor encodes three umbrella particles with distinct toxin and lectin composition. Notably, supernatant containing these toxins specifically and potently inhibits the growth of select Streptomyces species from among a diverse collection of bacteria screened. For one target, Streptomyces griseus, inhibition relies on a single toxin and that intoxication manifests as rapid cessation of vegetative hyphal growth. Our data show that Streptomyces umbrella particles mediate competition among vegetative mycelia of related species, a function distinct from small-molecule antibiotics, which are produced at the onset of reproductive growth and act broadly3,4. Sequence analyses suggest that this role of umbrella particles extends beyond Streptomyces, as we identified umbrella loci in nearly 1,000 species across Actinobacteria.

Suggested Citation

  • Qinqin Zhao & Savannah Bertolli & Young-Jun Park & Yongjun Tan & Kevin J. Cutler & Pooja Srinivas & Kyle L. Asfahl & Citlali Fonesca-García & Larry A. Gallagher & Yaqiao Li & Yaxi Wang & Devin Coleman, 2024. "Streptomyces umbrella toxin particles block hyphal growth of competing species," Nature, Nature, vol. 629(8010), pages 165-173, May.
  • Handle: RePEc:nat:nature:v:629:y:2024:i:8010:d:10.1038_s41586-024-07298-z
    DOI: 10.1038/s41586-024-07298-z
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