Starvation induces shrinkage of the bacterial cytoplasm

Abstract

Environmental fluctuations are a common challenge for single-celled organisms; enteric bacteria such as Escherichia coli experience dramatic changes in nutrient availability, pH, and temperature during their journey into and out of the host. While the effects of altered nutrient availability on gene expression and protein synthesis are well known, their impacts on cytoplasmic dynamics and cell morphology have been largely overlooked. Here, we discover that depletion of utilizable nutrients results in shrinkage of E. coli’s inner membrane from the cell wall. Shrinkage was accompanied by an ∼17% reduction in cytoplasmic volume and a concurrent increase in periplasmic volume. Inner membrane retraction after sudden starvation occurred almost exclusively at the new cell pole. This phenomenon was distinct from turgor-mediated plasmolysis and independent of new transcription, translation, or canonical starvation-sensing pathways. Cytoplasmic dry-mass density increased during shrinkage, suggesting that it is driven primarily by loss of water. Shrinkage was reversible: upon a shift to nutrient-rich medium, expansion started almost immediately at a rate dependent on carbon source quality. A robust entry into and recovery from shrinkage required the Tol-Pal system, highlighting the importance of envelope coupling during shrinkage and recovery. Klebsiella pneumoniae also exhibited shrinkage when shifted to carbon-free conditions, suggesting a conserved phenomenon. These findings demonstrate that even when Gram-negative bacterial growth is arrested, cell morphology and physiology are still dynamic.

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

“…S19 and Movie S6 ), in agreement with previous reports ( 40 ). Plasmolysis was recently also reported upon complete starvation ( 41 ). Therefore, turgor depends on the nutrient-dependent energy state of the cell.…”

Polyphosphate affects cytoplasmic and chromosomal dynamics in nitrogen-starved Pseudomonas aeruginosa

“…The nucleoid is thought to be a major contributor to the effective mesh size of the cytoplasm, and it has been shown in some bacterial species and conditions to compact during starvation (4). Cell volume in WT P. aeruginosa cells also decreases, which may contribute to overall crowding, and increased cytoplasmic density has been reported in E. coli under some starvation conditions (9). We have previously shown that ∆polyP cells fail to exit the cell cycle during nitrogen starvation, and therefore remain as large as WT growing cells (16).…”

“…These changes are thought to be driven by decreased transcription and increased synthesis of starvation-specific nucleoid associated structural proteins (NAPs) (5)(6)(7)(8). Meanwhile, the cytoplasm exhibits an overall decrease in volume and increase in density in some bacteria as well as in yeast (9,10). In some cases, changes in the dynamics of cytoplasmic components have also been observed (10,11).…”

Dietary Isothiocyanates, Sulforaphane and 2-Phenethyl Isothiocyanate, Effectively Impair Vibrio cholerae Virulence

“…It has been proposed that cytosol shrinkage might be one of the results of cell starvation [ 40 ]. According to Shi and colleagues, the condensation of cytoplasm is a natural feature of cells experiencing nutrient depletion.…”