Temporal segregation of biosynthetic processes is responsible for metabolic oscillations during the budding yeast cell cycle
Open accessAbstract
Many cell biological and biochemical mechanisms controlling the fundamental process of eukaryotic cell division have been identified; however, the temporal dynamics of biosynthetic processes during the cell division cycle are still elusive. Here, we show that key biosynthetic processes are temporally segregated along the cell cycle. Using budding yeast as a model and single-cell methods to dynamically measure metabolic activity, we observe two peaks in protein synthesis, in the G1 and S/G2/M phase, whereas lipid and polysaccharide synthesis peaks only once, during the S/G2/M phase. Integrating the inferred biosynthetic rates into a thermodynamic-stoichiometric metabolic model, we find that this temporal segregation in biosynthetic processes causes flux changes in primary metabolism, with an acceleration of glucose-uptake flux in G1 and phase-shifted oscillations of oxygen and carbon dioxide exchanges. Through experimental validation of the model predictions, we demonstrate that primary metabolism oscillates with cell-cycle periodicity to satisfy the changing demands of biosynthetic processes exhibiting unexpected dynamics during the cell cycle.
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The faster growth of the metabolically activated sub-population suggests that a conducive metabolic state drives cell division rather than cell-cycle progression driving metabolic responses.
“suggesting that a conducive metabolic state drives cell division rather than vice versa (cell-cycle progression driving metabolic responses8)”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [8]
The citation is attached to the parenthetical claim that cell-cycle progression drives metabolic responses, not to the citing authors’ conclusion about faster-growing cells. In the Discussion (page unavailable), the source says biosynthetic and metabolic oscillations are ‘at least not primarily’ generated by cell-cycle activity; it instead links changes in primary metabolism to changing biosynthetic demands. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredThe cell cycle is an example of a rhythmic signaling cascade, but coupling metabolism to it would constrain metabolic activation to specific stages of the cell cycle.
“One example is the cell cycle,8 but this arrangement would constrain metabolic activation to specific stages of the cell cycle, which may not necessarily deliver the best matching between metabolic demand and supply, particularly during longer phases of the cycle.”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [8]
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Self-citation
- Authors
- Takhaveev, V., Özsezen, S., Smith, E. N., Zylstra, A., Chaillet, M. L., Chen, H., Papagiannakis, A., Milias-Argeitis, A., & Heinemann, M.
- Affiliations
- University of Groningen (NL)
- Netherlands Organisation for Applied Scientific Research (NL)
- Corresponding author
- Heinemann, Matthias
- ORCID
- Venue
- Nature Metabolism
- Published
- 2023-02-27
- Volume
- 5
- Issue
- 2
- Pages
- 294-313
- ISSN
- 2522-5812 (ISSN-L)
- PMC
- PMC9970877
- OpenAlex
- W4322494372
- Cited by
- 36
- References
- 87
- Citations by year
- 2026: 9 · 2025: 7 · 2024: 13 · 2023: 7
- FWCI
- 3.21
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Metabolism (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
- TNO Repository (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Funders
- European Commission (642738, 847675)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (VI.C.192.003)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- cell cycle, metabolic oscillations, protein synthesis, lipogenesis, polysaccharide synthesis, glucose uptake, oxygen exchange, CO2 flux, primary metabolism, Saccharomyces cerevisiae
- MeSH terms
- Biological Transport, Cell Cycle, Cell Division, Saccharomycetales, Oxygen
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