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Extensive Regulation of Metabolism and Growth during the Cell Division Cycle

Nikolai Slavov, David Botstein, Amy Caudy
doi: https://doi.org/10.1101/005629
Nikolai Slavov
1Departments of Physics and Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
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David Botstein
2Lewis-Sigler Institute for Integrative Genomics and Molecular Biology Department, Princeton University, Princeton, NJ 08544, USA
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Amy Caudy
3Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, M5S 3E1, Canada
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Abstract

Yeast cells grown in culture can spontaneously synchronize their respiration, metabolism, gene expression and cell division. Such metabolic oscillations in synchronized cultures reflect single-cell oscillations, but the relationship between the oscillations in single cells and synchronized cultures is poorly understood. To understand this relationship and the coordination between metabolism and cell division, we collected and analyzed DNA-content, gene-expression and physiological data, at hundreds of time-points, from cultures metabolically-synchronized at different growth rates, carbon sources and biomass densities. The data enabled us to extend and generalize our mechanistic model, based on ensemble average over phases (EAP), connecting the population-average geneexpression of asynchronous cultures to the gene-expression dynamics in the single-cells comprising the cultures. The extended model explains the carbon-source specific growth-rate responses of hundreds of genes. Our physiological data demonstrate that the frequency of metabolic cycling in synchronized cultures increases with the biomass density, suggesting that this cycling is an emergent behavior, resulting from the entraining of the single-cell metabolic cycle by a quorum-sensing mechanism, and thus underscoring the difference between metabolic cycling in single cells and in synchronized cultures. Measurements of constant levels of residual glucose across metabolically synchronized cultures indicate that storage carbohydrates are required to fuel not only the G1/S transition of the division cycle but also the metabolic cycle. Despite the large variation in profiled conditions and in the scale of their dynamics, most genes preserve invariant dynamics of coordination with each other and with the rate of oxygen consumption. Similarly, the G1/S transition always occurs at the beginning, middle or end of the high oxygen consumption phases, analogous to observations in human and drosophila cells. These results highlight evolutionary conserved coordination among metabolism, cell growth and division.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 28, 2014.
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Extensive Regulation of Metabolism and Growth during the Cell Division Cycle
Nikolai Slavov, David Botstein, Amy Caudy
bioRxiv 005629; doi: https://doi.org/10.1101/005629
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Extensive Regulation of Metabolism and Growth during the Cell Division Cycle
Nikolai Slavov, David Botstein, Amy Caudy
bioRxiv 005629; doi: https://doi.org/10.1101/005629

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