IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48834-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48834-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48834-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Friedrich Fauser & Bhakti N. Kadam & Sebastian Arangundy-Franklin & Jessica E. Davis & Vishvesha Vaidya & Nicola J. Schmidt & Garrett Lew & Danny F. Xia & Rakshaa Mureli & Colman Ng & Yuanyue Zhou & N, 2024. "Compact zinc finger architecture utilizing toxin-derived cytidine deaminases for highly efficient base editing in human cells," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Dandan Wang & Lingfang Zhu & Xiangkai Zhen & Daoyan Yang & Changfu Li & Yating Chen & Huannan Wang & Yichen Qu & Xiaozhen Liu & Yanling Yin & Huawei Gu & Lei Xu & Chuanxing Wan & Yao Wang & Songying O, 2022. "A secreted effector with a dual role as a toxin and as a transcriptional factor," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Amaia González-Magaña & Igor Tascón & Jon Altuna-Alvarez & María Queralt-Martín & Jake Colautti & Carmen Velázquez & Maialen Zabala & Jessica Rojas-Palomino & Marité Cárdenas & Antonio Alcaraz & John , 2023. "Structural and functional insights into the delivery of a bacterial Rhs pore-forming toxin to the membrane," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Matthieu Haudiquet & Julie Bris & Amandine Nucci & Rémy A. Bonnin & Pilar Domingo-Calap & Eduardo P. C. Rocha & Olaya Rendueles, 2024. "Capsules and their traits shape phage susceptibility and plasmid conjugation efficiency," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Massimiliano Marazzato & Daniela Scribano & Meysam Sarshar & Francesca Brunetti & Silvia Fillo & Antonella Fortunato & Florigio Lista & Anna Teresa Palamara & Carlo Zagaglia & Cecilia Ambrosi, 2022. "Genetic Diversity of Antimicrobial Resistance and Key Virulence Features in Two Extensively Drug-Resistant Acinetobacter baumannii Isolates," IJERPH, MDPI, vol. 19(5), pages 1-14, March.
    7. Alexander Belyy & Philipp Heilen & Philine Hagel & Oliver Hofnagel & Stefan Raunser, 2023. "Structure and activation mechanism of the Makes caterpillars floppy 1 toxin," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48834-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.