Modeling the synchronization of yeast respiratory oscillations.

The budding yeast Saccharomyces cerevisiae exhibits autonomous oscillations when grown aerobically in continuous culture with ethanol as the primary carbon source. A single cell model that includes the sulfate assimilation and ethanol degradation pathways recently has been developed to study these respiratory oscillations. We utilize an extended version of this single cell model to construct large cell ensembles for investigation of a proposed synchronization mechanism involving hydrogen sulfide. Ensembles with as many as 10,000 cells are used to simulate population synchronization and to compute transient number distributions from asynchronous initial cell states. Random perturbations in intracellular kinetic parameters are introduced to study the synchronization of single cells with small variations in their unsynchronized oscillation periods. The cell population model is shown to be consistent with available experimental data and to provide insights into the regulatory mechanisms responsible for the synchronization of yeast metabolic oscillations.

[1]  M. Reuss,et al.  Cyclic AMP mediates the cell cycle dynamics of energy metabolism in Saccharomyces cerevisiae , 2003, Yeast.

[2]  Barbara M. Bakker,et al.  Acetaldehyde mediates the synchronization of sustained glycolytic oscillations in populations of yeast cells. , 1996, European journal of biochemistry.

[3]  J. Nielsen,et al.  Bioreaction Engineering Principles , 1994, Springer US.

[4]  H. Kuriyama,et al.  Synchronization affector of autonomous short‐period‐sustained oscillation of Saccharomyces cerevisiae , 1996, Yeast.

[5]  J. Nielsen,et al.  Population balance models of autonomous microbial oscillations. , 1995, Journal of biotechnology.

[6]  H. Sohn,et al.  Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide mediates population synchrony , 2000, Yeast.

[7]  H. Sohn,et al.  Ultradian metabolic oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide, a population synchronizer, is produced by sulphite reductase , 2001, Yeast.

[8]  M. Shuler,et al.  A structured, segregated model for genetically modified Escherichia coli cells and its use for prediction of plasmid stability , 1990, Biotechnology and bioengineering.

[9]  M M Domach,et al.  A finite representation model for an asynchronous culture of E. coli , 1984, Biotechnology and bioengineering.

[10]  Barbara M. Bakker,et al.  How yeast cells synchronize their glycolytic oscillations: a perturbation analytic treatment. , 2000, Biophysical journal.

[11]  Reinhart Heinrich,et al.  Transduction of intracellular and intercellular dynamics in yeast glycolytic oscillations. , 2000, Biophysical journal.

[12]  Britton Chance,et al.  Biological and biochemical oscillators , 1973 .

[13]  H. Meyenburg.  STABLE SYNCHRONY OSCILLATIONS IN CONTINUOUS CULTURES OF SACCHAROMYCES CEREVISIAE UNDER GLUCOSE LIMITATION , 1973 .

[14]  H. Kuriyama,et al.  Extracellular signaling in an oscillatory yeast culture , 1998 .

[15]  R. Heinrich,et al.  Mathematical analysis of a mechanism for autonomous metabolic oscillations in continuous culture of Saccharomyces cerevisiae , 2001, FEBS letters.

[16]  M. Holcombe,et al.  Information Processing in Cells and Tissues , 1998, Springer US.

[17]  Barbara M. Bakker,et al.  Yeast cells with a specific cellular make‐up and an environment that removes acetaldehyde are prone to sustained glycolytic oscillations , 1994, FEBS letters.

[18]  H. Kuriyama,et al.  Autonomous metabolic oscillation in continuous culture of Saccharomyces cerevisiae grown on ethanol. , 1996, FEMS microbiology letters.

[19]  H. Kuriyama,et al.  Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. , 1992, FEMS microbiology letters.

[20]  Hans V. Westerhoff,et al.  Synchrony and mutual stimulation of yeast cells during fast glycolytic oscillations , 1992 .

[21]  M. A. Henson.  Dynamic modeling of microbial cell populations. , 2003, Current opinion in biotechnology.

[22]  Reinhart Heinrich,et al.  Dynamics of two-component biochemical systems in interacting cells; synchronization and desynchronization of oscillations and multiple steady states. , 1997, Bio Systems.

[23]  A. Goldbeter,et al.  A Model for Circadian Rhythms in Drosophila Incorporating the Formation of a Complex between the PER and TIM Proteins , 1998, Journal of biological rhythms.

[24]  S. Strogatz,et al.  Synchronization of pulse-coupled biological oscillators , 1990 .

[25]  J Das,et al.  Analysis of the dynamics of relaxation type oscillation in glycolysis of yeast extracts. , 1991, Biophysical journal.

[26]  G. D. Byrne,et al.  VODE: a variable-coefficient ODE solver , 1989 .

[27]  Michael A. Henson,et al.  Dynamic modeling and control of yeast cell populations in continuous biochemical reactors , 2003, Comput. Chem. Eng..

[28]  Sibel Roller,et al.  Clock Control of Ultradian Respiratory Oscillation Found during Yeast Continuous Culture , 2001, Journal of bacteriology.

[29]  H C Lim,et al.  Induction and elimination of oscillations in continuous cultures of Saccharomyces cerevisiae , 1986, Biotechnology and bioengineering.

[30]  Matthias Reuss,et al.  Cell population modelling of yeast glycolytic oscillations. , 2002, The Biochemical journal.

[31]  A. Ghosh,et al.  Oscillations of glycolytic intermediates in yeast cells. , 1964, Biochemical and biophysical research communications.

[32]  R. Braatz,et al.  Measurement of particle size distribution in suspension polymerization using in situ laser backscattering , 2003 .

[33]  Doraiswami Ramkrishna,et al.  Statistics and dynamics of procaryotic cell populations , 1967 .

[34]  Reinhart Heinrich,et al.  Effect of cellular interaction on glycolytic oscillations in yeast: a theoretical investigation. , 2000, The Biochemical journal.

[35]  B Chance,et al.  Metabolic coupling and synchronization of NADH oscillations in yeast cell populations. , 1971, Archives of biochemistry and biophysics.