期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：32
DOI：10.1073/pnas.2021416118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Intracellular biomass density is an important variable for cellular physiology. It defines the crowded state of the cytoplasm and thus influences macromolecular interactions and transport. To control density during growth, bacteria must expand their cell volumes in synchrony with biomass. The regulation of volume growth and biomass density remain fundamentally not understood—in bacteria or any other organism. Using advanced microscopy, we demonstrate that cells control dry-mass density indirectly through two independent processes. First, cells expand surface area, rather than volume, in proportion with biomass growth. Second, cell width is controlled independently, with an important influence of turgor pressure. Our findings overturn a long-standing paradigm of mass-density constancy in bacteria and reveal fundamental determinants of dry-mass density and shape.
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 nonsteady conditions. Furthermore, the regulation of dry-mass density is fundamentally not understood in any organism. Using quantitative phase microscopy and an advanced 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 an empirical 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 slowly varying surface-to-mass coupling constant are the independent variables that determine dry-mass density.
