Streptomyces umbrella toxin particles block hyphal growth of competing species

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-Derr, Frank DiMaio, Dapeng Zhang, S. Brook Peterson, David Veesler and Joseph D. Mougous ()
Additional contact information
Qinqin Zhao: University of Washington
Savannah Bertolli: University of Washington
Young-Jun Park: University of Washington
Yongjun Tan: St Louis University
Kevin J. Cutler: University of Washington
Pooja Srinivas: University of Washington
Kyle L. Asfahl: University of Washington
Citlali Fonesca-García: USDA-ARS
Larry A. Gallagher: University of Washington
Yaqiao Li: University of Washington
Yaxi Wang: University of Washington
Devin Coleman-Derr: USDA-ARS
Frank DiMaio: University of Washington
Dapeng Zhang: St Louis University
S. Brook Peterson: University of Washington
David Veesler: University of Washington
Joseph D. Mougous: University of Washington

Nature, 2024, vol. 629, issue 8010, 165-173

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41586-024-07298-z

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