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Robust surface-to-mass coupling and turgor-dependent cell width determine bacterial dry-mass density

Citation

van Teeffelen, Sven; Oldewurtel, Enno Rainer; Kitahara, Yuki (2021), Robust surface-to-mass coupling and turgor-dependent cell width determine bacterial dry-mass density, Dryad, Dataset, https://doi.org/10.5061/dryad.zgmsbccbz

Abstract

During growth, cells must expand their cell volumes in coordination with biomass to control the level of cytoplasmic macromolecular crowding. Dry-mass density, the average ratio of dry mass to volume, is roughly constant between different nutrient conditions in bacteria, but it remains unknown whether cells maintain dry-mass density constant at the single-cell level and during non-steady conditions. Furthermore, the regulation of dry-mass density is fundamentally not understood in any organism. Using quantitative phase microscopy and a new image-analysis pipeline, we measured absolute single-cell mass and shape of the model organisms Escherichia coli and Caulobacter crescentus with improved precision and accuracy. We found that cells control dry-mass density indirectly, by expanding their surface, rather than volume, in direct proportion to biomass growth – according to a new surface growth law. At the same time, cell width is controlled independently. Therefore, cellular dry-mass density varies systematically with cell shape, both during the cell cycle or after nutrient shifts, while the surface-to-mass ratio remains nearly constant on the generation time scale. Transient deviations from constancy during nutrient shifts can be reconciled with turgor-pressure variations and the resulting elastic changes in surface area. Finally, we find that plastic changes of cell width after nutrient shifts are likely driven by turgor variations, demonstrating an important regulatory role of mechanical forces for width regulation. In conclusion, turgor-dependent cell width and a new, slowly varying surface-to-mass coupling constant are the independent variables that determine dry-mass density.

Funding

European Research Council, Award: 679980

Agence Nationale de la Recherche, Award: ANR-10-LABX-62-IBEID

Mairie de Paris, Award: Emergence(s) grant

Volkswagen Foundation

Mairie de Paris, Award: Emergence(s) grant