Involvement of a cell size control mechanism in the induction and maintenance of oscillations in continuous cultures of budding yeast

Abstract

Spontaneous oscillations occur in glucose-limited continuous cultures of Saccharomyces cerevisiae under aerobic conditions. The oscillatory behavior is detectable as a periodic change of many bioparameters such as dissolved oxygen, ethanol production, biomass concentration, as well as cellular content of storage carbohydrates and is associated to a marked synchronization of the yeast population. These oscillations may be related to a periodic accumulation of ethanol produced by yeast in the culture medium.The addition of ethanol to oscillating yeast cultures supports this hypothesis: indeed, no effect was observed if ethanol was added when already present in the medium, while a marked phase oscillation shift was obtained when ethanol was added at any other time. Moreover, the addition of ethanol to a nonoscillating culture triggers new oscillations. An accurate analysis performed at the level of nonoscillating yeast populations perturbed by addition of ethanol showed that both the growth rate and the protein content required for cell division increased in the presence of mixed substrate (i.e., ethanol plus limiting glucose). A marked synchronization of the yeast population occurred when the added ethanol was exhausted and the culture resumed growth only on limiting glucose. A decrease of protein content required for cell division was also apparent. These experimental findings support a new model for spontaneous oscillations in yeast cultures in which the alternative growth on limiting glucose and limiting glucose plus ethanol modifies the critical protein content required for cell division.

Cycles, phase synchronization, and entrainment in single-species phytoplankton populations

“…We observed the characteristic dynamics of the phase distribution only if we included coupling to the nutrient pool via a nutrient-sensitive and nonsensitive phase interval. Similar types of synchronization (yet at much shorter period lengths of several minutes and hours) have been observed in yeast cell cultures where glycolytic (31) or cell-cycle-dependent (32,33) oscillations became synchronized through the concentration of extracellular substrates and in nanochemostats where bacterial cells regulated cell density through a feedback mechanism based on quorum sensing of a signaling molecule (15).…”

Real-time luminescence monitoring of cell-cycle and respiratory oscillations in yeast

“…Acetaldehyde and ethanol may serve as synchronizing agents for oscillating respiration in continuous cultures because they are rhythmically released from yeast cells and they can strongly reset the phase of the YROs (19,31). We wanted to know whether these phase altering substances also alter the timing of cell division associated with the YROs.…”

“…The former phenomenon is intrinsic to all cells, but the observation of YROs has been limited to several strains of Saccharomyces cerevisiae that grow under specific conditions of continuous culture. Although the phenomenon has been known for decades (17), laboratories are only now beginning to elucidate the mechanisms underlying its stability and maintenance of population synchrony (18)(19)(20)(21). A coincidence between the CDC and YROs has been described (20,22) but the relationship between these two rhythmic phenomena is unclear (23,24).…”

Coupling of the cell cycle and metabolism in yeast cell-cycle-related oscillations via resource criticality and checkpoint gating

“…Here we propose a particular mechanism for signalling that is not via the production of any specific chemical agent or agents but rather through criticality of resources coupled with the engagement of a cell cycle checkpoint. Our hypothesis is an elaboration on the ideas in Martegani, Porro, Ranzi, and Alberghina (1990) where it was proposed that cell cycle 'partial synchronization' in the experiments occurs because fluctuations in ethanol and other metabolites raise and lower thresholds for initiation of budding and division. Rotenberg (1977) proposed that periodic gating of cells in a cell cycle could produce a clustered population structure.…”