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Contractile injection systems facilitate sporogenic differentiation of Streptomyces davawensis through the action of a phage tapemeasure protein-related effector

Author

Listed:
  • Toshiki Nagakubo

    (University of Tsukuba
    University of Tsukuba)

  • Tatsuya Nishiyama

    (Nihon University)

  • Tatsuya Yamamoto

    (University of Tsukuba)

  • Nobuhiko Nomura

    (University of Tsukuba
    University of Tsukuba
    University of Tsukuba)

  • Masanori Toyofuku

    (University of Tsukuba
    University of Tsukuba)

Abstract

Contractile injection systems (CISs) are prokaryotic phage tail-like nanostructures loading effector proteins that mediate various biological processes. Although CIS functions have been diversified through evolution and hold the great potential as protein delivery systems, the functional characterisation of CISs and their effectors is currently limited to a few CIS lineages. Here, we show that the CISs of Streptomyces davawensis belong to a unique group of bacterial CISs distributed across distant phyla and facilitate sporogenic differentiation of this bacterium. CIS loss results in decreases in extracellular DNA release, biomass accumulation, and spore formation in S. davawensis. CISs load an effector, which is a remote homolog of phage tapemeasure proteins, and its C-terminal domain has endonuclease activity responsible for the CIS-associated phenotypes. Our findings illustrate that CISs can contribute to the reproduction of bacteria through the action of the effector and suggest an evolutionary link between CIS effectors and viral cargos.

Suggested Citation

  • Toshiki Nagakubo & Tatsuya Nishiyama & Tatsuya Yamamoto & Nobuhiko Nomura & Masanori Toyofuku, 2024. "Contractile injection systems facilitate sporogenic differentiation of Streptomyces davawensis through the action of a phage tapemeasure protein-related effector," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48834-9
    DOI: 10.1038/s41467-024-48834-9
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    References listed on IDEAS

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    1. Alistair B. Russell & Rachel D. Hood & Nhat Khai Bui & Michele LeRoux & Waldemar Vollmer & Joseph D. Mougous, 2011. "Type VI secretion delivers bacteriolytic effectors to target cells," Nature, Nature, vol. 475(7356), pages 343-347, July.
    2. Alexander Martin Geller & Inbal Pollin & David Zlotkin & Aleks Danov & Nimrod Nachmias & William B. Andreopoulos & Keren Shemesh & Asaf Levy, 2021. "The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Joseph Kreitz & Mirco J. Friedrich & Akash Guru & Blake Lash & Makoto Saito & Rhiannon K. Macrae & Feng Zhang, 2023. "Programmable protein delivery with a bacterial contractile injection system," Nature, Nature, vol. 616(7956), pages 357-364, April.
    4. Maria Vladimirov & Ruo Xi Zhang & Stefanie Mak & Justin R. Nodwell & Alan R. Davidson, 2023. "A contractile injection system is required for developmentally regulated cell death in Streptomyces coelicolor," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
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