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Coupling among growth rate response, metabolic cycle, and cell division cycle in yeast.

Slavov N, Botstein D - Mol. Biol. Cell (2011)

Bottom Line: All genes with universal GRR, which comprise 25% of the genome, are expressed periodically in the yeast metabolic cycle (YMC).This idea is supported by oxygen consumption data from metabolically synchronized cultures with doubling times ranging from 5 to 14 h.We found that the high oxygen consumption phase of the YMC can coincide exactly with the S phase of the cell division cycle, suggesting that oxidative metabolism and DNA replication are not incompatible.

View Article: PubMed Central - PubMed

Affiliation: Massachusetts Institute of Technology, Cambridge, MA 02139, USA. nslavov@alum.mit.edu

ABSTRACT
We studied the steady-state responses to changes in growth rate of yeast when ethanol is the sole source of carbon and energy. Analysis of these data, together with data from studies where glucose was the carbon source, allowed us to distinguish a "universal" growth rate response (GRR) common to all media studied from a GRR specific to the carbon source. Genes with positive universal GRR include ribosomal, translation, and mitochondrial genes, and those with negative GRR include autophagy, vacuolar, and stress response genes. The carbon source-specific GRR genes control mitochondrial function, peroxisomes, and synthesis of vitamins and cofactors, suggesting this response may reflect the intensity of oxidative metabolism. All genes with universal GRR, which comprise 25% of the genome, are expressed periodically in the yeast metabolic cycle (YMC). We propose that the universal GRR may be accounted for by changes in the relative durations of the YMC phases. This idea is supported by oxygen consumption data from metabolically synchronized cultures with doubling times ranging from 5 to 14 h. We found that the high oxygen consumption phase of the YMC can coincide exactly with the S phase of the cell division cycle, suggesting that oxidative metabolism and DNA replication are not incompatible.

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Physiological responses to growth rate on ethanol (A–D) and on glucose (E–F), (Brauer et al., 2008). All responses are plotted as a function of the growth rate across the nutrient limitations indicated in the legends. (A) Biomass in ethanol carbon source; (B) residual ethanol concentration; (C) bud index in ethanol carbon source; (D) duration of the budded phase in ethanol carbon source; (E) bud index in glucose carbon source; (F) duration of the budded phase in glucose carbon source.
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Figure 1: Physiological responses to growth rate on ethanol (A–D) and on glucose (E–F), (Brauer et al., 2008). All responses are plotted as a function of the growth rate across the nutrient limitations indicated in the legends. (A) Biomass in ethanol carbon source; (B) residual ethanol concentration; (C) bud index in ethanol carbon source; (D) duration of the budded phase in ethanol carbon source; (E) bud index in glucose carbon source; (F) duration of the budded phase in glucose carbon source.

Mentions: In the ethanol cultures at steady-state, the cell density (Figure 1A) decreases monotonically with increasing growth rate, similar to the results of Brauer et al. (2008) for the analogous experiments with glucose as carbon source. This is entirely consistent with theoretical expectations, as described in the Supplementary Material. The concentrations of residual ethanol in the fermenter vessels also follow the expected trend. As the flux of medium is reduced, cells grow more slowly and spend more time in the reaction vessels. Both of these factors suggest that the concentration of residual ethanol should be inversely correlated to the growth rate of the cultures, as we observed (Figure 1B). The specific consumption of ethanol (i.e., ethanol consumed/steady-state biomass) is lower for the ethanol-limited cultures (C), suggesting that cultures limited on phosphate (P) or ammonium (N) might metabolize some fraction of the excess ethanol to acetate, possibly to generate reducing NADPH required for biosynthetic processes.


Coupling among growth rate response, metabolic cycle, and cell division cycle in yeast.

Slavov N, Botstein D - Mol. Biol. Cell (2011)

Physiological responses to growth rate on ethanol (A–D) and on glucose (E–F), (Brauer et al., 2008). All responses are plotted as a function of the growth rate across the nutrient limitations indicated in the legends. (A) Biomass in ethanol carbon source; (B) residual ethanol concentration; (C) bud index in ethanol carbon source; (D) duration of the budded phase in ethanol carbon source; (E) bud index in glucose carbon source; (F) duration of the budded phase in glucose carbon source.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3113766&req=5

Figure 1: Physiological responses to growth rate on ethanol (A–D) and on glucose (E–F), (Brauer et al., 2008). All responses are plotted as a function of the growth rate across the nutrient limitations indicated in the legends. (A) Biomass in ethanol carbon source; (B) residual ethanol concentration; (C) bud index in ethanol carbon source; (D) duration of the budded phase in ethanol carbon source; (E) bud index in glucose carbon source; (F) duration of the budded phase in glucose carbon source.
Mentions: In the ethanol cultures at steady-state, the cell density (Figure 1A) decreases monotonically with increasing growth rate, similar to the results of Brauer et al. (2008) for the analogous experiments with glucose as carbon source. This is entirely consistent with theoretical expectations, as described in the Supplementary Material. The concentrations of residual ethanol in the fermenter vessels also follow the expected trend. As the flux of medium is reduced, cells grow more slowly and spend more time in the reaction vessels. Both of these factors suggest that the concentration of residual ethanol should be inversely correlated to the growth rate of the cultures, as we observed (Figure 1B). The specific consumption of ethanol (i.e., ethanol consumed/steady-state biomass) is lower for the ethanol-limited cultures (C), suggesting that cultures limited on phosphate (P) or ammonium (N) might metabolize some fraction of the excess ethanol to acetate, possibly to generate reducing NADPH required for biosynthetic processes.

Bottom Line: All genes with universal GRR, which comprise 25% of the genome, are expressed periodically in the yeast metabolic cycle (YMC).This idea is supported by oxygen consumption data from metabolically synchronized cultures with doubling times ranging from 5 to 14 h.We found that the high oxygen consumption phase of the YMC can coincide exactly with the S phase of the cell division cycle, suggesting that oxidative metabolism and DNA replication are not incompatible.

View Article: PubMed Central - PubMed

Affiliation: Massachusetts Institute of Technology, Cambridge, MA 02139, USA. nslavov@alum.mit.edu

ABSTRACT
We studied the steady-state responses to changes in growth rate of yeast when ethanol is the sole source of carbon and energy. Analysis of these data, together with data from studies where glucose was the carbon source, allowed us to distinguish a "universal" growth rate response (GRR) common to all media studied from a GRR specific to the carbon source. Genes with positive universal GRR include ribosomal, translation, and mitochondrial genes, and those with negative GRR include autophagy, vacuolar, and stress response genes. The carbon source-specific GRR genes control mitochondrial function, peroxisomes, and synthesis of vitamins and cofactors, suggesting this response may reflect the intensity of oxidative metabolism. All genes with universal GRR, which comprise 25% of the genome, are expressed periodically in the yeast metabolic cycle (YMC). We propose that the universal GRR may be accounted for by changes in the relative durations of the YMC phases. This idea is supported by oxygen consumption data from metabolically synchronized cultures with doubling times ranging from 5 to 14 h. We found that the high oxygen consumption phase of the YMC can coincide exactly with the S phase of the cell division cycle, suggesting that oxidative metabolism and DNA replication are not incompatible.

Show MeSH