Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast

  1. Pascal D Odermatt
  2. Teemu P Miettinen
  3. Joel Lemiere
  4. Joon Ho Kang
  5. Emrah Bostan
  6. Scott R Manalis
  7. Kerwyn Casey Huang
  8. Fred Chang  Is a corresponding author
  1. UCSF, United States
  2. Massachusetts Institute of Technology, United States
  3. Korea Institute of Science and Technology, Republic of Korea
  4. University of Amsterdam, Netherlands
  5. Stanford University, United States

Abstract

Intracellular density impacts the physical nature of the cytoplasm and can globally affect cellular processes, yet density regulation remains poorly understood. Here, using a new quantitative phase imaging method, we determined that dry-mass density in fission yeast is maintained in a narrow distribution and exhibits homeostatic behavior. However, density varied during the cell cycle, decreasing during G2, increasing in mitosis and cytokinesis, and dropping rapidly at cell birth. These density variations were explained by a constant rate of biomass synthesis, coupled to slowdown of volume growth during cell division and rapid expansion post-cytokinesis. Arrest at specific cell-cycle stages exacerbated density changes. Spatially heterogeneous patterns of density suggested links between density regulation, tip growth, and intracellular osmotic pressure. Our results demonstrate that systematic density variations during the cell cycle are predominantly due to modulation of volume expansion, and reveal functional consequences of density gradients and cell-cycle arrests.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Custom Matlab code used for image analysis has been posted online at the Github repository https://bitbucket.org/kchuanglab/quantitative-phase-imaging/src/master/.

Article and author information

Author details

  1. Pascal D Odermatt

    Department of Cell and Tissue Biology, UCSF, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Teemu P Miettinen

    Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5975-200X
  3. Joel Lemiere

    Department of Cell and Tissue Biology, UCSF, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Joon Ho Kang

    Brain Science Institute, Korea Institute of Science and Technology, Seoul, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4165-7538
  5. Emrah Bostan

    Informatics Institute, University of Amsterdam, Amsterdamn, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Scott R Manalis

    Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Kerwyn Casey Huang

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8043-8138
  8. Fred Chang

    Department of Cell and Tissue Biology, UCSF, San Francisco, United States
    For correspondence
    fred.chang@ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8907-3286

Funding

Swiss National Foundation (P2ELP3_172318)

  • Pascal D Odermatt

Swiss National Foundation (P400PB_180872)

  • Pascal D Odermatt

National Institute of General Medical Sciences (NIH GM056836)

  • Fred Chang

Wellcome Trust (110275/Z/15/Z)

  • Teemu P Miettinen

Chan Zuckerberg Initiative

  • Kerwyn Casey Huang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mohan K Balasubramanian, University of Warwick, United Kingdom

Publication history

  1. Received: November 14, 2020
  2. Accepted: June 7, 2021
  3. Accepted Manuscript published: June 8, 2021 (version 1)
  4. Version of Record published: June 23, 2021 (version 2)

Copyright

© 2021, Odermatt et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Pascal D Odermatt
  2. Teemu P Miettinen
  3. Joel Lemiere
  4. Joon Ho Kang
  5. Emrah Bostan
  6. Scott R Manalis
  7. Kerwyn Casey Huang
  8. Fred Chang
(2021)
Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast
eLife 10:e64901.
https://doi.org/10.7554/eLife.64901
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