IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33054-w.html
   My bibliography  Save this article

Endocytosis-like DNA uptake by cell wall-deficient bacteria

Author

Listed:
  • Renée Kapteijn

    (Leiden University)

  • Shraddha Shitut

    (Leiden University)

  • Dennis Aschmann

    (Leiden Institute of Chemistry, Leiden University)

  • Le Zhang

    (Leiden University)

  • Marit Beer

    (Radboudumc Technology Center Microscopy)

  • Deniz Daviran

    (Radboudumc Technology Center Microscopy)

  • Rona Roverts

    (Radboudumc Technology Center Microscopy)

  • Anat Akiva

    (Radboudumc Technology Center Microscopy)

  • Gilles P. Wezel

    (Leiden University)

  • Alexander Kros

    (Leiden Institute of Chemistry, Leiden University)

  • Dennis Claessen

    (Leiden University)

Abstract

Horizontal gene transfer in bacteria is widely believed to occur via conjugation, transduction and transformation. These mechanisms facilitate the passage of DNA across the protective cell wall using sophisticated machinery. Here, we report that cell wall-deficient bacteria can engulf DNA and other extracellular material via an endocytosis-like process. Specifically, we show that L-forms of the filamentous actinomycete Kitasatospora viridifaciens can take up plasmid DNA, polysaccharides (dextran) and 150-nm lipid nanoparticles. The process involves invagination of the cytoplasmic membrane, leading to formation of intracellular vesicles that encapsulate extracellular material. DNA uptake is not affected by deletion of genes homologous to comEC and comEA, which are required for natural transformation in other species. However, uptake is inhibited by sodium azide or incubation at 4 °C, suggesting the process is energy-dependent. The encapsulated materials are released into the cytoplasm upon degradation of the vesicle membrane. Given that cell wall-deficient bacteria are considered a model for early life forms, our work reveals a possible mechanism for primordial cells to acquire food or genetic material before invention of the bacterial cell wall.

Suggested Citation

  • Renée Kapteijn & Shraddha Shitut & Dennis Aschmann & Le Zhang & Marit Beer & Deniz Daviran & Rona Roverts & Anat Akiva & Gilles P. Wezel & Alexander Kros & Dennis Claessen, 2022. "Endocytosis-like DNA uptake by cell wall-deficient bacteria," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33054-w
    DOI: 10.1038/s41467-022-33054-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33054-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33054-w?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. M. Leaver & P. Domínguez-Cuevas & J. M. Coxhead & R. A. Daniel & J. Errington, 2009. "Life without a wall or division machine in Bacillus subtilis," Nature, Nature, vol. 457(7231), pages 849-853, February.
    2. M. Leaver & P. Domínguez-Cuevas & J. M. Coxhead & R. A. Daniel & J. Errington, 2009. "Erratum: Life without a wall or division machine in Bacillus subtilis," Nature, Nature, vol. 460(7254), pages 538-538, July.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Joshua N. Hamm & Yan Liao & Andriko Kügelgen & Nina Dombrowski & Evan Landers & Christopher Brownlee & Emma M. V. Johansson & Renee M. Whan & Matthew A. B. Baker & Buzz Baum & Tanmay A. M. Bharat & Ia, 2024. "The parasitic lifestyle of an archaeal symbiont," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    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. Simone Pelliciari & Salomé Bodet-Lefèvre & Stepan Fenyk & Daniel Stevens & Charles Winterhalter & Frederic D. Schramm & Sara Pintar & Daniel R. Burnham & George Merces & Tomas T. Richardson & Yumiko T, 2023. "The bacterial replication origin BUS promotes nucleobase capture," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Yoshikazu Kawai & Maki Kawai & Eilidh Sohini Mackenzie & Yousef Dashti & Bernhard Kepplinger & Kevin John Waldron & Jeff Errington, 2023. "On the mechanisms of lysis triggered by perturbations of bacterial cell wall biosynthesis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Manuel Halte & Ekaterina P. Andrianova & Christian Goosmann & Fabienne F. V. Chevance & Kelly T. Hughes & Igor B. Zhulin & Marc Erhardt, 2024. "FlhE functions as a chaperone to prevent formation of periplasmic flagella in Gram-negative bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Miloš Tišma & Florian Patrick Bock & Jacob Kerssemakers & Hammam Antar & Aleksandre Japaridze & Stephan Gruber & Cees Dekker, 2024. "Direct observation of a crescent-shape chromosome in expanded Bacillus subtilis cells," Nature Communications, Nature, vol. 15(1), pages 1-13, 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:13:y:2022:i:1:d:10.1038_s41467-022-33054-w. 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.