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

Author:

Odermatt Pascal D12ORCID,Miettinen Teemu P34ORCID,Lemière Joël1ORCID,Kang Joon Ho356ORCID,Bostan Emrah7,Manalis Scott R389,Huang Kerwyn Casey21011ORCID,Chang Fred1ORCID

Affiliation:

1. Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United States

2. Department of Bioengineering, Stanford University, Stanford, United States

3. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States

4. MRC Laboratory for Molecular Cell Biology, University College, London, United Kingdom

5. Department of Physics, Massachusetts Institute of Technology, Cambridge, United States

6. Brain Science Institute, Korea Institute of Science and Technology, Seoul, Republic of Korea

7. Informatics Institute, University of Amsterdam, Amsterdamn, Netherlands

8. Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, United States

9. Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, United States

10. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, United States

11. Chan Zuckerberg Biohub, San Francisco, 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.

Funder

Swiss National Science Foundation

National Institute of General Medical Sciences

Wellcome Trust

Chan Zuckerberg Initiative

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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