Homeostasis of cytoplasmic crowding by cell wall fluidization and ribosomal counterions

TL;DR

Cells maintain cytoplasmic balance by adjusting turgor pressure through ribosomal RNA counterions, coordinating cell wall expansion and biomass density.

Contribution

A novel mechanism linking ribosomal RNA counterions to turgor pressure control, coordinating cell wall expansion and biomass homeostasis.

Findings

Turgor pressure increases with growth rate in E. coli, yet biomass density remains constant.

Mathematical modeling shows cell wall fluidization explains turgor and biomass density coordination.

Ribosomal RNA counterions directly control turgor pressure, linking cytoplasmic and cell wall processes.

Abstract

In bacteria, algae, fungi, and plant cells, the wall must expand in concert with cytoplasmic biomass production, otherwise cells would experience toxic molecular crowding1,2 or lyse. But how cells achieve expansion of this complex biomaterial in coordination with biosynthesis of macromolecules in the cytoplasm remains unexplained3, although recent works have revealed that these processes are indeed coupled4,5. Here, we report a striking increase of turgor pressure with growth rate in E. coli, suggesting that the speed of cell wall expansion is controlled via turgor. Remarkably, despite this increase in turgor pressure, cellular biomass density remains constant across a wide range of growth rates. By contrast, perturbations of turgor pressure that deviate from this scaling directly alter biomass density. A mathematical model based on cell wall fluidization by cell wall endopeptidases not only explains these apparently confounding observations but makes surprising quantitative predictions that we validated experimentally. The picture that emerges is that turgor pressure is directly controlled via counterions of ribosomal RNA. Elegantly, the coupling between rRNA and turgor pressure simultaneously coordinates cell wall expansion across a wide range of growth rates and exerts homeostatic feedback control on biomass density. This mechanism may regulate cell wall biosynthesis from microbes to plants and has important implications for the mechanism of action of antibiotics6.

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