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Free energy rhythms in Saccharomyces cerevisiae: a dynamic perspective with implications for ribosomal biogenesis.

ABSTRACT: To describe the time course of cellular systems, we integrate ideas from thermodynamics and information theory to discuss the work needed to change the state of the cell. The biological example analyzed is experimental microarray transcription level oscillations of yeast in the different phases as characterized by oxygen consumption. Surprisal analysis was applied to identify groups of transcripts that oscillate in concert and thereby to compute changes in free energy with time. Three dominant transcript groups were identified by surprisal analysis. The groups correspond to the respiratory, early, and late reductive phases. Genes involved in ribosome biogenesis peaked at the respiratory phase. The work to prepare the state is shown to be the sum of the contributions of these groups. We paid particular attention to work requirements during ribosomal building, and the correlation with ATP levels and dissolved oxygen. The suggestion that cells in the respiratory phase likely build ribosomes, an energy intensive process, in preparation for protein production during the S phase of the cell cycle is validated by an experiment. Surprisal analysis thereby provided a useful tool for determining the synchronization of transcription events and energetics in a cell in real time.

SUBMITTER: Gross A

PROVIDER: S-EPMC3655800 | biostudies-literature | 2013 Mar

REPOSITORIES: biostudies-literature

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Free energy rhythms in Saccharomyces cerevisiae: a dynamic perspective with implications for ribosomal biogenesis.

Gross A A Li Caroline M CM Remacle F F Levine R D RD

Biochemistry 20130220 9

To describe the time course of cellular systems, we integrate ideas from thermodynamics and information theory to discuss the work needed to change the state of the cell. The biological example analyzed is experimental microarray transcription level oscillations of yeast in the different phases as characterized by oxygen consumption. Surprisal analysis was applied to identify groups of transcripts that oscillate in concert and thereby to compute changes in free energy with time. Three dominant t ...[more]

PMID: 23379300

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Project description:BackgroundThe concerted effects of changes in gene expression due to changes in the environment are ultimately reflected in the metabolome. Dynamics of metabolite concentrations under a certain condition can therefore give a description of the cellular state with a high degree of functional information. We used this potential to evaluate the metabolic status of two recombinant strains of Saccharomyces cerevisiae during anaerobic batch fermentation of a glucose/xylose mixture. Two isogenic strains were studied, differing only in the pathways used for xylose assimilation: the oxidoreductive pathway with xylose reductase (XR) and xylitol dehydrogenase (XDH) or the isomerization pathway with xylose isomerase (XI). The isogenic relationship between the two strains ascertains that the observed responses are a result of the particular xylose pathway and not due to unknown changes in regulatory systems. An increased understanding of the physiological state of these strains is important for further development of efficient pentose-utilizing strains for bioethanol production.ResultsUsing LC-MS/MS we determined the dynamics in the concentrations of intracellular metabolites in central carbon metabolism, nine amino acids, the purine nucleotides and redox cofactors. The general response to the transition from glucose to xylose was increased concentrations of amino acids and TCA-cycle intermediates, and decreased concentrations of sugar phosphates and redox cofactors. The two strains investigated had significantly different uptake rates of xylose which led to an enhanced response in the XI-strain. Despite the difference in xylose uptake rate, the adenylate energy charge remained high and stable around 0.8 in both strains. In contrast to the adenylate pool, large changes were observed in the guanylate pool.ConclusionsThe low uptake of xylose by the XI-strain led to several distinguished responses: depletion of key metabolites in glycolysis and NADPH, a reduced GTP/GDP ratio and accumulation of PEP and aromatic amino acids. These changes are strong indicators of carbon starvation. The XR/XDH-strain displayed few such traits. The coexistence of these traits and a stable adenylate charge indicates that xylose supplies energy to the cells but does not suppress a response similar to carbon starvation. Particular signals may play a role in the latter, of which the GTP/GMP ratio could be a candidate as it decreased significantly in both strains.

Dataset Information

Free energy rhythms in Saccharomyces cerevisiae: a dynamic perspective with implications for ribosomal biogenesis.

Publications

Free energy rhythms in Saccharomyces cerevisiae: a dynamic perspective with implications for ribosomal biogenesis.

Similar Datasets

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