Abstract
Trehalose and glycogen accumulate in Saccharomyces cerevisiae when growth conditions deteriorate. It has been suggested that aside from functioning as storage factors and stress protectants, these carbohydrates may be required for cell cycle progression at low growth rates under carbon limitation. By using a mutant unable to synthesize trehalose and glycogen, we have investigated this requirement of trehalose and glycogen under carbon-limited conditions in continuous cultures. Trehalose and glycogen levels increased with decreasing growth rates in the wild-type strain, whereas no trehalose or glycogen was detected in the mutant. However, the mutant was still able to grow and divide at low growth rates with doubling times similar to those for the wild-type strain, indicating that trehalose and glycogen are not essential for cell cycle progression. Nevertheless, upon a slight increase of extracellular carbohydrates, the wild-type strain degraded its reserve carbohydrates and was able to enter a cell division cycle faster than the mutant. In addition, wild-type cells survived much longer than the mutant cells when extracellular carbon was exhausted. Thus, trehalose and glycogen have a dual role under these conditions, serving as storage factors during carbon starvation and providing quickly a higher carbon and ATP flux when conditions improve. Interestingly, the CO2 production rate and hence the ATP flux were higher in the mutant than in the wild-type strain at low growth rates. The possibility that the mutant strain requires this steady higher glycolytic flux at low growth rates for passage through Start is discussed.
MeSH Terms
Biomass
Cell Cycle/physiology
Cell Division
Galactose/metabolism
Glycogen/metabolism
Kinetics
Saccharomyces cerevisiae/cytology,genetics,physiology
Trehalose/metabolism
Chemicals
Glycogen
Trehalose
Galactose
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Silljé H H
Department of Molecular Cell Biology, Utrecht University, 3584 CH Utrecht, The Netherlands.
Paalman J W
ter Schure E G
Olsthoorn S Q
Verkleij A J
Boonstra J
Verrips C T
References (23)
23 references, click to expand
-
Multiple effects of trehalose on protein folding in vitro and in vivo.
Mol Cell. 1998 Apr;1(5):639-48
PMID: 9660948
-
Cyclin partners determine Pho85 protein kinase substrate specificity in vitro and in vivo: control of glycogen biosynthesis by Pcl8 and Pcl10.
Mol Cell Biol. 1998 Jun;18(6):3289-99
PMID: 9584169
-
Trehalose in yeast, stress protectant rather than reserve carbohydrate.
Antonie Van Leeuwenhoek. 1990 Oct;58(3):209-17
PMID: 2256682
-
Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation.
J Bacteriol. 1980 Sep;143(3):1384-94
PMID: 6997270
-
Preservation of membranes in anhydrobiotic organisms: the role of trehalose.
Science. 1984 Feb 17;223(4637):701-3
PMID: 17841031
-
Trehalose synthase: guard to the gate of glycolysis in yeast?
Trends Biochem Sci. 1995 Jan;20(1):3-10
PMID: 7878741
-
Cell cycle control by a complex of the cyclin HCS26 (PCL1) and the kinase PHO85.
Science. 1994 Nov 25;266(5189):1388-91
PMID: 7973730
-
Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation.
Eur J Biochem. 1992 Nov 1;209(3):951-9
PMID: 1425702
-
The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro.
Eur J Biochem. 1994 Jan 15;219(1-2):187-93
PMID: 8306985
-
Signal transduction in yeast.
Yeast. 1994 Dec;10(13):1753-90
PMID: 7747517
-
The PCL2 (ORFD)-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast.
Science. 1994 Nov 25;266(5189):1391-5
PMID: 7973731
-
Effects of different carbon fluxes on G1 phase duration, cyclin expression, and reserve carbohydrate metabolism in Saccharomyces cerevisiae.
J Bacteriol. 1997 Nov;179(21):6560-5
PMID: 9352900
-
Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae.
J Bacteriol. 1987 Dec;169(12):5518-22
PMID: 2960663
-
Deletion of the gene encoding the cyclin-dependent protein kinase Pho85 alters glycogen metabolism in Saccharomyces cerevisiae.
Genetics. 1996 May;143(1):57-66
PMID: 8722762
-
Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae.
Prog Nucleic Acid Res Mol Biol. 1998;58:197-237
PMID: 9308367
-
Analysis of transcription and translation of glycolytic enzymes in glucose-limited continuous cultures of Saccharomyces cerevisiae.
J Gen Microbiol. 1992 Dec;138(12):2559-66
PMID: 1487726
-
The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII.
Curr Genet. 1993;23(4):281-9
PMID: 8467527
-
Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose.
Microbiology. 1997 Jun;143 ( Pt 6):1891-900
PMID: 9202465
-
Pho85p, a cyclin-dependent protein kinase, and the Snf1p protein kinase act antagonistically to control glycogen accumulation in Saccharomyces cerevisiae.
Mol Cell Biol. 1996 Aug;16(8):4357-65
PMID: 8754836
-
Two glycogen synthase isoforms in Saccharomyces cerevisiae are coded by distinct genes that are differentially controlled.
J Biol Chem. 1991 Aug 25;266(24):15602-7
PMID: 1908457
-
Changes in carbohydrate composition and trehalase-activity during the budding cycle of Saccharomyces cerevisiae.
Arch Mikrobiol. 1969;64(4):396-407
PMID: 4916776
-
Isolation of the GSY1 gene encoding yeast glycogen synthase and evidence for the existence of a second gene.
J Biol Chem. 1990 Dec 5;265(34):20879-86
PMID: 2123485
-
The Cdc25 protein of Saccharomyces cerevisiae is required for normal glucose transport.
Microbiology. 1996 Jul;142 ( Pt 7):1765-73
PMID: 8757740