IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47094-x.html
   My bibliography  Save this article

Direct observation of a crescent-shape chromosome in expanded Bacillus subtilis cells

Author

Listed:
  • Miloš Tišma

    (Kavli Institute of Nanoscience Delft, Delft University of Technology)

  • Florian Patrick Bock

    (Faculty of Biology and Medicine (FBM), University of Lausanne (UNIL))

  • Jacob Kerssemakers

    (Kavli Institute of Nanoscience Delft, Delft University of Technology)

  • Hammam Antar

    (Faculty of Biology and Medicine (FBM), University of Lausanne (UNIL))

  • Aleksandre Japaridze

    (Kavli Institute of Nanoscience Delft, Delft University of Technology)

  • Stephan Gruber

    (Faculty of Biology and Medicine (FBM), University of Lausanne (UNIL))

  • Cees Dekker

    (Kavli Institute of Nanoscience Delft, Delft University of Technology)

Abstract

Bacterial chromosomes are folded into tightly regulated three-dimensional structures to ensure proper transcription, replication, and segregation of the genetic information. Direct visualization of chromosomal shape within bacterial cells is hampered by cell-wall confinement and the optical diffraction limit. Here, we combine cell-shape manipulation strategies, high-resolution fluorescence microscopy techniques, and genetic engineering to visualize the shape of unconfined bacterial chromosome in real-time in live Bacillus subtilis cells that are expanded in volume. We show that the chromosomes predominantly exhibit crescent shapes with a non-uniform DNA density that is increased near the origin of replication (oriC). Additionally, we localized ParB and BsSMC proteins – the key drivers of chromosomal organization – along the contour of the crescent chromosome, showing the highest density near oriC. Opening of the BsSMC ring complex disrupted the crescent chromosome shape and instead yielded a torus shape. These findings help to understand the threedimensional organization of the chromosome and the main protein complexes that underlie its structure.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47094-x
    DOI: 10.1038/s41467-024-47094-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47094-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47094-x?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. F. Kunst & N. Ogasawara & I. Moszer & A. M. Albertini & G. Alloni & V. Azevedo & M. G. Bertero & P. Bessières & A. Bolotin & S. Borchert & R. Borriss & L. Boursier & A. Brans & M. Braun & S. C. Brigne, 1997. "The complete genome sequence of the Gram-positive bacterium Bacillus subtilis," Nature, Nature, vol. 390(6657), pages 249-256, November.
    2. Fabai Wu & Aleksandre Japaridze & Xuan Zheng & Jakub Wiktor & Jacob W. J. Kerssemakers & Cees Dekker, 2019. "Direct imaging of the circular chromosome in a live bacterium," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    3. 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.
    4. 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.
    5. Remus T. Dame & Maarten C. Noom & Gijs J. L. Wuite, 2006. "Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation," Nature, Nature, vol. 444(7117), pages 387-390, November.
    6. Aleksandre Japaridze & Christos Gogou & Jacob W. J. Kerssemakers & Huyen My Nguyen & Cees Dekker, 2020. "Direct observation of independently moving replisomes in Escherichia coli," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    7. Marie Trussart & Eva Yus & Sira Martinez & Davide Baù & Yuhei O. Tahara & Thomas Pengo & Michael Widjaja & Simon Kretschmer & Jim Swoger & Steven Djordjevic & Lynne Turnbull & Cynthia Whitchurch & Mak, 2017. "Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    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. 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.
    2. David Geisel & Peter Lenz, 2022. "Machine learning classification of trajectories from molecular dynamics simulations of chromosome segregation," PLOS ONE, Public Library of Science, vol. 17(1), pages 1-33, January.
    3. 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.
    4. 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.
    5. Shuyu Li & Qinmeng Liu & Chongyi Duan & Jialin Li & Hengxi Sun & Lei Xu & Qiao Yang & Yao Wang & Xihui Shen & Lei Zhang, 2023. "c-di-GMP inhibits the DNA binding activity of H-NS in Salmonella," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Vikash Kumar & Nikhil Raghuvanshi & Abhay K. Pandey & Abhishek Kumar & Emily Thoday-Kennedy & Surya Kant, 2023. "Role of Halotolerant Plant Growth-Promoting Rhizobacteria in Mitigating Salinity Stress: Recent Advances and Possibilities," Agriculture, MDPI, vol. 13(1), pages 1-22, January.
    7. Fatema-Zahra M. Rashid & Frédéric G. E. Crémazy & Andreas Hofmann & David Forrest & David C. Grainger & Dieter W. Heermann & Remus T. Dame, 2023. "The environmentally-regulated interplay between local three-dimensional chromatin organisation and transcription of proVWX in E. coli," Nature Communications, Nature, vol. 14(1), pages 1-25, December.
    8. David Forrest & Emily A. Warman & Amanda M. Erkelens & Remus T. Dame & David C. Grainger, 2022. "Xenogeneic silencing strategies in bacteria are dictated by RNA polymerase promiscuity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Alicia Broto & Erika Gaspari & Samuel Miravet-Verde & Vitor A. P. Martins Santos & Mark Isalan, 2022. "A genetic toolkit and gene switches to limit Mycoplasma growth for biosafety applications," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. Chen Zhang & Asha Mary Joseph & Laurent Casini & Justine Collier & Anjana Badrinarayanan & Suliana Manley, 2024. "Chromosome organization shapes replisome dynamics in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-12, 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_s41467-024-47094-x. 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.