IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39513-2.html
   My bibliography  Save this article

Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division

Author

Listed:
  • Beatrice Ramm

    (Max Planck Institute of Biochemistry
    Princeton University)

  • Dominik Schumacher

    (Max Planck Institute for Terrestrial Microbiology)

  • Andrea Harms

    (Max Planck Institute for Terrestrial Microbiology)

  • Tamara Heermann

    (Max Planck Institute of Biochemistry)

  • Philipp Klos

    (Max Planck Institute for Terrestrial Microbiology)

  • Franziska Müller

    (Max Planck Institute for Terrestrial Microbiology)

  • Petra Schwille

    (Max Planck Institute of Biochemistry)

  • Lotte Søgaard-Andersen

    (Max Planck Institute for Terrestrial Microbiology)

Abstract

Cell division is spatiotemporally precisely regulated, but the underlying mechanisms are incompletely understood. In the social bacterium Myxococcus xanthus, the PomX/PomY/PomZ proteins form a single megadalton-sized complex that directly positions and stimulates cytokinetic ring formation by the tubulin homolog FtsZ. Here, we study the structure and mechanism of this complex in vitro and in vivo. We demonstrate that PomY forms liquid-like biomolecular condensates by phase separation, while PomX self-assembles into filaments generating a single large cellular structure. The PomX structure enriches PomY, thereby guaranteeing the formation of precisely one PomY condensate per cell through surface-assisted condensation. In vitro, PomY condensates selectively enrich FtsZ and nucleate GTP-dependent FtsZ polymerization and bundle FtsZ filaments, suggesting a cell division site positioning mechanism in which the single PomY condensate enriches FtsZ to guide FtsZ-ring formation and division. This mechanism shares features with microtubule nucleation by biomolecular condensates in eukaryotes, supporting this mechanism’s ancient origin.

Suggested Citation

  • Beatrice Ramm & Dominik Schumacher & Andrea Harms & Tamara Heermann & Philipp Klos & Franziska Müller & Petra Schwille & Lotte Søgaard-Andersen, 2023. "Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39513-2
    DOI: 10.1038/s41467-023-39513-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39513-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39513-2?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. Bernardo Gouveia & Yoonji Kim & Joshua W. Shaevitz & Sabine Petry & Howard A. Stone & Clifford P. Brangwynne, 2022. "Capillary forces generated by biomolecular condensates," Nature, Nature, vol. 609(7926), pages 255-264, September.
    2. Aurore Fleurie & Christian Lesterlin & Sylvie Manuse & Chao Zhao & Caroline Cluzel & Jean-Pierre Lavergne & Mirita Franz-Wachtel & Boris Macek & Christophe Combet & Erkin Kuru & Michael S. VanNieuwenh, 2014. "MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae," Nature, Nature, vol. 516(7530), pages 259-262, December.
    3. Matthew R. King & Sabine Petry, 2020. "Phase separation of TPX2 enhances and spatially coordinates microtubule nucleation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Pilong Li & Sudeep Banjade & Hui-Chun Cheng & Soyeon Kim & Baoyu Chen & Liang Guo & Marc Llaguno & Javoris V. Hollingsworth & David S. King & Salman F. Banani & Paul S. Russo & Qiu-Xing Jiang & B. Tra, 2012. "Phase transitions in the assembly of multivalent signalling proteins," Nature, Nature, vol. 483(7389), pages 336-340, March.
    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. María Pérez-Burgos & Marco Herfurth & Andreas Kaczmarczyk & Andrea Harms & Katrin Huber & Urs Jenal & Timo Glatter & Lotte Søgaard-Andersen, 2024. "A deterministic, c-di-GMP-dependent program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis," Nature Communications, Nature, vol. 15(1), pages 1-20, 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. Etienne Jambon-Puillet & Andrea Testa & Charlotta Lorenz & Robert W. Style & Aleksander A. Rebane & Eric R. Dufresne, 2024. "Phase-separated droplets swim to their dissolution," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Mina Farag & Wade M. Borcherds & Anne Bremer & Tanja Mittag & Rohit V. Pappu, 2023. "Phase separation of protein mixtures is driven by the interplay of homotypic and heterotypic interactions," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Agustín Mangiarotti & Nannan Chen & Ziliang Zhao & Reinhard Lipowsky & Rumiana Dimova, 2023. "Wetting and complex remodeling of membranes by biomolecular condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Maruša Ramšak & Dominique A. Ramirez & Loren E. Hough & Michael R. Shirts & Sara Vidmar & Kristina Eleršič Filipič & Gregor Anderluh & Roman Jerala, 2023. "Programmable de novo designed coiled coil-mediated phase separation in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Jun Sun & Jiale Qu & Cai Zhao & Xinyao Zhang & Xinyu Liu & Jia Wang & Chao Wei & Xinyi Liu & Mulan Wang & Pengguihang Zeng & Xiuxiao Tang & Xiaoru Ling & Li Qing & Shaoshuai Jiang & Jiahao Chen & Tara, 2024. "Precise prediction of phase-separation key residues by machine learning," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Furqan Dar & Samuel R. Cohen & Diana M. Mitrea & Aaron H. Phillips & Gergely Nagy & Wellington C. Leite & Christopher B. Stanley & Jeong-Mo Choi & Richard W. Kriwacki & Rohit V. Pappu, 2024. "Biomolecular condensates form spatially inhomogeneous network fluids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Shuangcheng Alivia Wu & Chenchen Shen & Xiaoqiong Wei & Xiawei Zhang & Siwen Wang & Xinxin Chen & Mauricio Torres & You Lu & Liangguang Leo Lin & Huilun Helen Wang & Allen H. Hunter & Deyu Fang & Shen, 2023. "The mechanisms to dispose of misfolded proteins in the endoplasmic reticulum of adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Zheng Shen & Daxiao Sun & Adriana Savastano & Sára Joana Varga & Maria-Sol Cima-Omori & Stefan Becker & Alf Honigmann & Markus Zweckstetter, 2023. "Multivalent Tau/PSD-95 interactions arrest in vitro condensates and clusters mimicking the postsynaptic density," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. Halima H. Schede & Pradeep Natarajan & Arup K. Chakraborty & Krishna Shrinivas, 2023. "A model for organization and regulation of nuclear condensates by gene activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. Omar A. Saleh & Sam Wilken & Todd M. Squires & Tim Liedl, 2023. "Vacuole dynamics and popping-based motility in liquid droplets of DNA," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    11. Manisha Poudyal & Komal Patel & Laxmikant Gadhe & Ajay Singh Sawner & Pradeep Kadu & Debalina Datta & Semanti Mukherjee & Soumik Ray & Ambuja Navalkar & Siddhartha Maiti & Debdeep Chatterjee & Jyoti D, 2023. "Intermolecular interactions underlie protein/peptide phase separation irrespective of sequence and structure at crowded milieu," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    12. Mengru Yang & Nicolas Wenner & Gregory F. Dykes & Yan Li & Xiaojun Zhu & Yaqi Sun & Fang Huang & Jay C. D. Hinton & Lu-Ning Liu, 2022. "Biogenesis of a bacterial metabolosome for propanediol utilization," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    13. Min Lee & Hyungseok C. Moon & Hyeonjeong Jeong & Dong Wook Kim & Hye Yoon Park & Yongdae Shin, 2024. "Optogenetic control of mRNA condensation reveals an intimate link between condensate material properties and functions," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Takayuki Miki & Masahiro Hashimoto & Hiroki Takahashi & Masatoshi Shimizu & Sae Nakayama & Tadaomi Furuta & Hisakazu Mihara, 2024. "De novo designed YK peptides forming reversible amyloid for synthetic protein condensates in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Agustín Mangiarotti & Macarena Siri & Nicky W. Tam & Ziliang Zhao & Leonel Malacrida & Rumiana Dimova, 2023. "Biomolecular condensates modulate membrane lipid packing and hydration," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    16. Taehyun Kim & Jaeyoon Yoo & Sungho Do & Dong Soo Hwang & YongKeun Park & Yongdae Shin, 2023. "RNA-mediated demixing transition of low-density condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Andrew Z. Lin & Kiersten M. Ruff & Furqan Dar & Ameya Jalihal & Matthew R. King & Jared M. Lalmansingh & Ammon E. Posey & Nadia A. Erkamp & Ian Seim & Amy S. Gladfelter & Rohit V. Pappu, 2023. "Dynamical control enables the formation of demixed biomolecular condensates," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Jason X. Liu & Mikko P. Haataja & Andrej Košmrlj & Sujit S. Datta & Craig B. Arnold & Rodney D. Priestley, 2023. "Liquid–liquid phase separation within fibrillar networks," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    19. Cheng Qi & Xudong Ma & Qi Zeng & Zhangwei Huang & Shanshan Zhang & Xiaokang Deng & Tiantian Kong & Zhou Liu, 2024. "Multicompartmental coacervate-based protocell by spontaneous droplet evaporation," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    20. Song Xue & Fan Zhou & Tian Zhao & Huimin Zhao & Xuewei Wang & Long Chen & Jin-ping Li & Shi-Zhong Luo, 2022. "Phase separation on cell surface facilitates bFGF signal transduction with heparan sulphate," Nature Communications, Nature, vol. 13(1), pages 1-10, 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:14:y:2023:i:1:d:10.1038_s41467-023-39513-2. 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.