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Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density in Bacillus subtilis

Yuki Kitahara, Enno R. Oldewurtel, Sean Wilson, Ethan C. Garner, View ORCID ProfileSven van Teeffelen
doi: https://doi.org/10.1101/2021.05.05.442853
Yuki Kitahara
1Département de Microbiologie, Infectiologie, et Immunologie, Faculté de Médecine, Université de Montréal, Montréal, QC, Canada
2Microbial Morphogenesis and Growth Lab, Institut Pasteur, Paris
3Université de Paris, Paris, France
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Enno R. Oldewurtel
2Microbial Morphogenesis and Growth Lab, Institut Pasteur, Paris
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Sean Wilson
4Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
5Center for Systems Biology, Harvard University, Cambridge, United States
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Ethan C. Garner
4Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
5Center for Systems Biology, Harvard University, Cambridge, United States
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Sven van Teeffelen
1Département de Microbiologie, Infectiologie, et Immunologie, Faculté de Médecine, Université de Montréal, Montréal, QC, Canada
2Microbial Morphogenesis and Growth Lab, Institut Pasteur, Paris
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  • ORCID record for Sven van Teeffelen
  • For correspondence: sven.vanteeffelen@gmail.com
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Abstract

Cells must increase their volumes in response to biomass growth to maintain intracellular mass density, the ratio of dry mass to cell volume, within physiologically permissive bounds. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. Recently, we demonstrated that the Gram-negative bacterium Escherichia coli expands cell-surface area rather than volume in proportion to mass. Here, we investigate the regulation of cell-volume growth in the evolutionarily distant Bacillus subtilis. First, we demonstrate that the coupling of surface growth to mass growth is conserved in B. subtilis. Therefore, mass density changes with cell shape at the single-cell level. Interestingly, mass density varies by more than 30% when we systematically change cell width by modulation of cell-wall insertion, without any effect on mass-growth rate. Second, we demonstrate that the coupling of surface- and mass growth is broken if peptidoglycan or membrane synthesis are inhibited. Once transient perturbations are relieved, the surface-to-mass ratio is rapidly restored. In conclusion, we demonstrate that surface-to-mass coupling is a conserved principle for volume regulation in bacteria, and that envelope synthesis provides an important link between surface growth and biomass growth in B. subtilis.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 06, 2021.
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Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density in Bacillus subtilis
Yuki Kitahara, Enno R. Oldewurtel, Sean Wilson, Ethan C. Garner, Sven van Teeffelen
bioRxiv 2021.05.05.442853; doi: https://doi.org/10.1101/2021.05.05.442853
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Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density in Bacillus subtilis
Yuki Kitahara, Enno R. Oldewurtel, Sean Wilson, Ethan C. Garner, Sven van Teeffelen
bioRxiv 2021.05.05.442853; doi: https://doi.org/10.1101/2021.05.05.442853

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