Changes in carbohydrate composition and trehalase-activity during the budding cycle of Saccharomyces cerevisiae

Küenzi, Martin; Fiechter, Armin

doi:10.1007/bf00417021

Cited by 130 publications

(85 citation statements)

References 23 publications

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“…Then the dissolved oxygen in the culture media returned to the level before inoculation (100%), indicating sudden and complete cessation of respiration. Subsequently, the oxygen level in the media and thus the consumption of the culture oscillated for many hours, just as seen in continuous cultures (4,10). We reproduced this synchronization in several independent cultures (SI Appendix, Fig.…”

Section: Resultssupporting

confidence: 60%

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Metabolic cycling without cell division cycling in respiring yeast

Slavov

Macinskas

Caudy

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

104

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Despite rapid progress in characterizing the yeast metabolic cycle, its connection to the cell division cycle (CDC) has remained unclear. We discovered that a prototrophic batch culture of budding yeast, growing in a phosphate-limited ethanol medium, synchronizes spontaneously and goes through multiple metabolic cycles, whereas the fraction of cells in the G1/G0 phase of the CDC increases monotonically from 90 to 99%. This demonstrates that metabolic cycling does not require cell division cycling and that metabolic synchrony does not require carbon-source limitation. More than 3,000 genes, including most genes annotated to the CDC, were expressed periodically in our batch culture, albeit a mere 10% of the cells divided asynchronously; only a smaller subset of CDC genes correlated with cell division. These results suggest that the yeast metabolic cycle reflects a growth cycle during G1/G0 and explains our previous puzzling observation that genes annotated to the CDC increase in expression at slow growth.T wo kinds of periodic behavior have been characterized in slowly growing yeast cultures. The first, the classical cell division cycle (CDC), consists of four phases (G0/G1, S, G2, and M) that are easily distinguished by morphological criteria. When the growth rate of budding yeast is slowed by mutations or chemicals inhibiting growth, the duration of the G1/G0 phase increases relative to the durations of the S, G2, and M phases (1). Recently, we confirmed and quantified this CDC trend (Fig. 1A) in chemostat cultures whose steady-state growth rate was controlled by limiting natural nutrients (2, 3). The second kind of cycle, the yeast metabolic cycle (YMC), was first observed more than four decades ago (4) as periodic oscillations in the oxygen consumption of continuous, glucose-limited cultures growing in a chemostat. Like the CDC, the YMC can be divided phenomenologically into two phases: the low oxygen consumption phase (LOC), when the amount of oxygen in the medium is high because the cells consume little oxygen, and the high oxygen consumption phase (HOC), when the reverse holds (SI Appendix). We also reported previously (3) similar growth-rate changes in the relative durations of the phases of the YMC (Fig. 1B). As the growth rate increases, the relative duration of the LOC decreases whereas the relative duration of the HOC increases (Fig. 1B), similarly to the analogous changes in the CDC.These changes in the relative durations of the phases affect the composition of asynchronous cultures, because single cells from asynchronous cultures cycle metabolically (5, 6) and thus the fraction of cells in a particular phase is proportional to the duration of that phase relative to the entire cycle period. The increase in the relative duration of a phase results in the increase in the fraction of cells in that phase, and thus an increase in the population-average expression levels of genes peaking during that phase. Consider, for example, a ribosomal gene that peaks in expression during the HOC phase; at slow growt...

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Section: Resultssupporting

confidence: 60%

“…Biosynthetic genes peak during the HOC phase, whereas autophagy and vacuolar genes peak during the LOC. In a continuous YMC culture, a fraction of the culture divides synchronously during each YMC period (4,10,11), indicating a coupling between the YMC and the CDC. However, the mechanism of this coupling remains unclear.…”

mentioning

confidence: 99%

Metabolic cycling without cell division cycling in respiring yeast

Slavov

Macinskas

Caudy

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

104

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“…The trehalose level might even be part of the system that gates entry into S phase of the cell-division cycle (29). The observation that growth on trehalose as the sole carbon source produces spontaneous metabolic cycling in batch cultures (22) may be relevant in this regard, as are the older observations that trehalose is metabolized preferentially during S phase of the cell-division cycle (30,31).…”

Section: Discussionmentioning

confidence: 99%

Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate

Silverman

Petti

Slavov

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Oscillations in patterns of expression of a large fraction of yeast genes are associated with the “metabolic cycle,” usually seen only in prestarved, continuous cultures of yeast. We used FISH of mRNA in individual cells to test the hypothesis that these oscillations happen in single cells drawn from unsynchronized cultures growing exponentially in chemostats. Gene-expression data from synchronized cultures were used to predict coincident appearance of mRNAs from pairs of genes in the unsynchronized cells. Quantitative analysis of the FISH results shows that individual unsynchronized cells growing slowly because of glucose limitation or phosphate limitation show the predicted oscillations. We conclude that the yeast metabolic cycle is an intrinsic property of yeast metabolism and does not depend on either synchronization or external limitation of growth by the carbon source.

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“…(2) Reliance was placed on data from washed suspensions without evidence that the results were relevant to normal growth conditions (Hommes, 1966;Giirts, 1967;Fales, 1960;Beran & Zemanova, 1969;Hoogerheide, 1971;Johnson et al, 1972;Silhankova et al, 1975). ( 3 ) There was a failure to achieve balanced growth under batch conditions (Beck & von Meyenburg, 1968;von Meyenburg, 1969) or to provide sufficient detail to substantiate the existence of balanced growth (De Deken, 1966;Kuenzi & Fiechter, 1969;Gorts, 1971 ;Silhankova et al, 1975 ;Lagunas, 1976). (4) Large random and systematic errors in the estimation of gas exchange data are possible unless very careful techniques are used (Fiechter, 1975;Barford & Hall, 1979b).…”

Section: Discussionmentioning

confidence: 99%

An Examination of the Crabtree Effect in Saccharomyces cerevisiae: the Role of Respiratory Adaptation

Barford¹,

Hall²

1979

Journal of General Microbiology

119

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The control of glycolysis and respiration in a strain of baker's yeast was quantified, including, for the first time, corrections obtained from carbon and redox balances which allowed for interactions between anabolism and catabolism. When these corrections were applied, no repression of respiration was observed during fully adapted growth in continuous culture ; however, the rate of respiration reached a maximum value, independent of the nature of the energy substrate, at a specific growth rate less than the maximum specific growth rate of the organism. During batch growth, considerable adaptation was necessary for this organism to achieve its maximum respiratory capacity. Further, this adaptation was extremely slow, particularly when glucose or maltose was the limiting substrate, and its full extent was frequently not achieved. Consequently, a residual repression, presumably originally caused by growth under restricted aeration in shake flasks, was observed during batch growth.

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Changes in carbohydrate composition and trehalase-activity during the budding cycle of Saccharomyces cerevisiae

Cited by 130 publications

References 23 publications

Metabolic cycling without cell division cycling in respiring yeast

Metabolic cycling without cell division cycling in respiring yeast

Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate

An Examination of the Crabtree Effect in Saccharomyces cerevisiae: the Role of Respiratory Adaptation

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