Biophysical properties of Saccharomyces cerevisiae and their relationship with HOG pathway activation

Abstract

Parameterized models of biophysical and mechanical cell properties are important for predictive mathematical modeling of cellular processes. The concepts of turgor, cell wall elasticity, osmotically active volume, and intracellular osmolarity have been investigated for decades, but a consistent rigorous parameterization of these concepts is lacking. Here, we subjected several data sets of minimum volume measurements in yeast obtained after hyper-osmotic shock to a thermodynamic modeling framework. We estimated parameters for several relevant biophysical cell properties and tested alternative hypotheses about these concepts using a model discrimination approach. In accordance with previous reports, we estimated an average initial turgor of 0.6 ± 0.2 MPa and found that turgor becomes negligible at a relative volume of 93.3 ± 6.3% corresponding to an osmotic shock of 0.4 ± 0.2 Osm/l. At high stress levels (4 Osm/l), plasmolysis may occur. We found that the volumetric elastic modulus, a measure of cell wall elasticity, is 14.3 ± 10.4 MPa. Our model discrimination analysis suggests that other thermodynamic quantities affecting the intracellular water potential, for example the matrix potential, can be neglected under physiological conditions. The parameterized turgor models showed that activation of the osmosensing high osmolarity glycerol (HOG) signaling pathway correlates with turgor loss in a 1:1 relationship. This finding suggests that mechanical properties of the membrane trigger HOG pathway activation, which can be represented and quantitatively modeled by turgor.Electronic supplementary materialThe online version of this article (doi:10.1007/s00249-010-0612-0) contains supplementary material, which is available to authorized users.

Severe osmotic compression triggers a slowdown of intracellular signaling, which can be explained by molecular crowding

“…2C). This is in agreement with Schaber et al, who proposed the minimum compression volume for yeast cells to be between 33% and 49% of their normal volume (10). The delays in both Hog1p phosphorylation and nuclear translocation correlated with the changes in cell volume: the smaller the cell volume (measured immediately after osmotic stress), the slower the dynamics of Hog1p phosphorylation and nuclear translocation (Fig.…”

“…In yeast, osmotic shrinkage is completed within a few tens of seconds after exposure to increased osmolarity (9). The final cell volume is set by the mechanical equilibration of external, internal, and turgor pressures (10,11). Hyperosmotic stress alters a variety of cellular processes, such as disrupting the cytoskeleton structure (12,13), inducing chromatin remodeling (14,15), and triggering cell cycle arrest (16,17) and apoptosis (18,19).…”

The indentation of pressurized elastic shells: from polymeric capsules to yeast cells

“…Using this result and typical estimates for the thickness of the cell wall h % 70 nm and cell radius R % 2.75 mm from the literature [6], we take the measured upper and lower bounds for k 1 (see dashed lines in figure 5a) and estimate that 12 MPa E 46 MPa. This value is reasonably consistent with values determined previously [5,30] and also gives ' p % 2 mm and ' b % 200 mm, which are both significantly larger than the AFM tip used ( 15 nm) justifying our approximation of a point force. With this value of E, the theory developed here, more specifically equation (3.6), can be used to estimate the internal pressure required to obtain the observed values of k 1 .…”

“…We find a typical value of turgor of 0.1 -0.2 MPa, which is consistent with experiments using different methodologies [30,31], which found turgor pressures in the range 0 -1 MPa. Finally, we note that for these experiments 0 t 10 and so it is necessary to make use of the full analytical expression (3.6).…”

Local Turgor Pressure Reduction via Channel Clustering

“…We estimate whether it is energetically favorable for a hemispherical invagination of radius of R i ¼ 30 nm (12) to form in the presence of accepted values of the turgor pressure. We take k ¼ 285 k B T (13), and P ¼ 0.6 MPa as an average over a number of measurements (14)(15)(16)(17)(18)(19). Then the stabilizing contribution from the curvature-generating proteins is ¼ À2pR…”