Reversible solidification of fission yeast cytoplasm after prolonged nutrient starvation

Abstract

Cells depend on a highly ordered organisation of their content and must develop strategies to maintain the anisotropic distribution of organelles during periods of nutrient shortage. One of these strategies is to solidify the cytoplasm, which was observed in bacteria and yeast cells with acutely interrupted energy production. Here, we describe a different type of cytoplasm solidification fission yeast cells switch to, after having run out of nutrients during multiple days in culture. It provides the most profound reversible cytoplasmic solidification of yeast cells described to date. Our data exclude the previously proposed mechanisms for cytoplasm solidification in yeasts and suggest a mechanism that immobilises cellular components in a size-dependent manner. We provide experimental evidence that, in addition to time, cells use intrinsic nutrients and energy sources to reach this state. Such cytoplasmic solidification may provide a robust means to protect cellular architecture in dormant cells.

Physical properties of the cytoplasm modulate the rates of microtubule polymerization and depolymerization

“…Rather, cells regulate and vary their density as part of normal cell physiology: during the cell cycle, among different cell types, aging, nutritional responses and disease states (Neurohr and Amon, 2020). There is evidence though that the density of cytoplasm may be near functional limits (Dill et al, 2011) as increasing its concentration can lead to large effects including solidification of the cytoplasm (Heimlicher et al, 2019; Joyner et al, 2016; Munder et al, 2016). These density changes, which potentially affect cytoplasmic concentration and crowding effects, further underscore the importance of understanding effects of cytoplasmic concentration.…”

Nuclear pores constrict upon energy depletion

“…This points to a well conserved mechanism, likely dependent on a concomitantly reduced availability of free GTP (27). Moreover, energy depletion (ED) leads to a general reorganization of the cytoplasm including solidification of the periplasm, general water loss and reduction of the nuclear and cellular volume, which allows cells to endure under unfavorable conditions (28)(29)(30)(31). If the shutdown of active nuclear transport coincides with the alteration in passive diffusion and potentially a conformational adaption of NPC architecture remains unknown.…”

Essential role of non-vesicular lipid transport in microtubule-controlled cell polarisation

“…The most plausible mechanism is that kes1p transports the newly synthesised sterols directly from their production site, the ER, to the plasma membrane. In fission yeast, these two membranes are closely aligned throughout the cell circumference, also in starved cells, which certainly facilitates such a mechanism 24,56 . Yet, at this stage we cannot fully exclude the involvement of an unidentified membrane organelle intermediate, acting prior to kes1p in a multi-step pathway.…”