Do yeast cells dream of metabolic sheep?

Rainer Machné

The YRO percolate throughout cellular physiology. Some of these dynamics differ between the short period YRO observed in the IFO 0233 strain, and longer period YRO, with a stronger coupling to the cell division cycle. Most importantly and often misunderstood (see PubPeer comments for Tu et al. (2005)), fermentation and glycogen cycling occur in opposite phases: glycogen is accumulated during the LOC phase (Küenzi and Fiechter 1969) and used to fuel the HOC phase, with a short peak of fermentation, in CDC-coupled YRO (Sonnleitner and Hahnemann 1994); but produced during the HOC and consumed during the fermentative LOC phase in short period YRO (Satroutdinov, Kuriyama, and Kobayashi (1992); Keulers, Satroutdinov, et al. (1996); DB Murray (1997/unpublished)). When grown on ethanol as carbon source, Keulers, Suzuki, et al. (1996) detected no glycogen at all during the YRO. This shows that the main mechanistic model of the YRO is not generally valid.

In contrast, ATP and specifically the ATP/ADP ratio has been consistently shown to peak in early HOC phase and reach a minimum in early LOC phase in both long period (Meyenburg 1969; Xu, Yaguchi, and Tsurugi 2004; Müller 2006) and short period YRO (Machné and Murray 2012; Amariei et al. 2014). Similarly, the pH is minimal in HOC and maximal in LOC phase in both (Keulers, Satroutdinov, et al. 1996; O' Neill et al. 2020).

Learn more about metabolic dynamics in the introduction to my lecture series, or in my PhD thesis (2017).

Data collection and scripts available via the ChemostatData git. Data by Küenzi and Fiechter (1969), Meyenburg (1969), Müller (2006), Chin et al. (2012), Keulers, Satroutdinov, et al. (1996), Satroutdinov, Kuriyama, and Kobayashi (1992), Sillje et al. (1999), Xu, Yaguchi, and Tsurugi (2004), Machné and Murray (2012), Amariei et al. (2014), and unpublished data by Douglas B. Murray (© 1997).

Glycogen Cycling and Fermentation

CDC-coupled

IFO 0233

ATP/ADP

CDC-coupled

IFO 0233

pH

IFO 0233

Biomass and Cell Cycle

CDC-coupled

IFO 0233

References

Amariei, C., R. Machné, V. Stolc, T. Soga, M. Tomita, and D. B. Murray. 2014. "Time Resolved DNA Occupancy Dynamics During the Respiratory Oscillation Uncover a Global Reset Point in the Yeast Growth Program." Microb Cell 1 (9): 279-88. https://doi.org/10.15698/mic2014.09.166.
Chin, S. L., I. M. Marcus, R. R. Klevecz, and C. M. Li. 2012. "Dynamics of Oscillatory Phenotypes in Saccharomyces Cerevisiae Reveal a Network of Genome-Wide Transcriptional Oscillators." FEBS J 279 (6): 1119-30. https://doi.org/10.1111/j.1742-4658.2012.08508.x.
Keulers, M., A. D. Satroutdinov, T. Suzuki, and H. Kuriyama. 1996. "Synchronization Affector of Autonomous Short-Period-Sustained Oscillation of Saccharomyces Cerevisiae." Yeast 12 (7): 673-82. https://doi.org/10.1002/(SICI)1097-0061(19960615)12:7<673::AID-YEA958>3.0.CO;2-C.
Keulers, M., T. Suzuki, A. D. Satroutdinov, and H. Kuriyama. 1996. "Autonomous Metabolic Oscillation in Continuous Culture of Saccharomyces Cerevisiae Grown on Ethanol." FEMS Microbiol Lett 142 (2-3): 253-58.
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Machné, R., and D. B. Murray. 2012. "The Yin and Yang of Yeast Transcription: Elements of a Global Feedback System Between Metabolism and Chromatin." PLoS One 7 (6): e37906. https://doi.org/10.1371/journal.pone.0037906.
Meyenburg, Kaspar von. 1969. "Katabolit-Repression und der Sprossungszyklus von Saccharomyces cerevisiae." Vierteljahrsschrift Der Naturforschenden Gesellschaft in Zürich. PhD thesis, ETH Zürich.
Müller, Dirk. 2006. "Model-Assisted Analysis of Cyclic AMP Signal Transduction in Saccharomyces Cerevisiae — cAMP as Dynamic Coordinator of Energy Metabolism and Cell Cycle Progression." PhD thesis, Universität Stuttgart.
O' Neill, J. S., N. P. Hoyle, J. B. Robertson, R. S. Edgar, A. D. Beale, S. Y. Peak-Chew, J. Day, A. S. H. Costa, C. Frezza, and H. C. Causton. 2020. "Eukaryotic Cell Biology Is Temporally Coordinated to Support the Energetic Demands of Protein Homeostasis." Nat Commun 11 (1): 4706. https://doi.org/10.1038/s41467-020-18330-x.
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Sillje, H. H., J. W. Paalman, E. G. ter Schure, S. Q. Olsthoorn, A. J. Verkleij, J. Boonstra, and C. T. Verrips. 1999. "Function of Trehalose and Glycogen in Cell Cycle Progression and Cell Viability in Saccharomyces Cerevisiae." J Bacteriol 181 (2): 396-400. https://doi.org/10.1128/JB.181.2.396-400.1999.
Sonnleitner, B., and U. Hahnemann. 1994. "Dynamics of the Respiratory Bottleneck of Saccharomyces Cerevisiae." Journal of Biotechnology 38 (1): 63-79. https://doi.org/http://dx.doi.org/10.1016/0168-1656(94)90148-1.
Tu, B. P., A. Kudlicki, M. Rowicka, and S. L. McKnight. 2005. "Logic of the Yeast Metabolic Cycle: Temporal Compartmentalization of Cellular Processes." Science 310 (5751): 1152-58.
Xu, Z., S. Yaguchi, and K. Tsurugi. 2004. "Gts1p Stabilizes Oscillations in Energy Metabolism by Activating the Transcription of TPS1 Encoding Trehalose-6-Phosphate Synthase 1 in the Yeast Saccharomyces Cerevisiae." Biochem J 383 (Pt 1): 171-78. https://doi.org/10.1042/BJ20040967.