Trehalose reserve in Saccharomyces cerevisiae: phenomenon of transport, accumulation and role in cell viability

Plourde-Owobi, Lucile; Durner, Sophie; Goma, G.; François, Jean

doi:10.1016/s0168-1605(00)00210-5

Cited by 37 publications

(24 citation statements)

References 26 publications

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“…Since Ath1p is essential for growth on trehalose in the absence of the Agt1p-Nth1p pathway (23), it was not possible to investigate this question using a tps1 nth1 nth2 mutant that was further defective in Ath1p. We circumvented this difficulty by cultivating the quadruple tps1 nth1 nth2 ath1 mutant in a galactose medium containing trehalose, since this medium is permissive for the growth of tps1 mutants and enables trehalose accumulation by Agt1p-mediated transport (35). Under this condition, the culture of the tps1 strain followed a biphasic growth ( Fig.…”

Section: Resultsmentioning

confidence: 99%

New Insights into Trehalose Metabolism by Saccharomyces cerevisiae : NTH2 Encodes a Functional Cytosolic Trehalase, and Deletion of TPS1 Reveals Ath1p-Dependent Trehalose Mobilization

Jules

Beltran

François

et al. 2008

Appl Environ Microbiol

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In the yeast Saccharomyces cerevisiae, the synthesis of endogenous trehalose is catalyzed by a trehalose synthase complex, TPS, and its hydrolysis relies on a cytosolic/neutral trehalase encoded by NTH1. In this work, we showed that NTH2, a paralog of NTH1, encodes a functional trehalase that is implicated in trehalose mobilization. Yeast is also endowed with an acid trehalase encoded by ATH1 and an H ؉ /trehalose transporter encoded by AGT1, which can together sustain assimilation of exogenous trehalose. We showed that a tps1 mutant defective in the TPS catalytic subunit cultivated on trehalose, or on a dual source of carbon made of galactose and trehalose, accumulated high levels of intracellular trehalose by its Agt1p-mediated transport. The accumulated disaccharide was mobilized as soon as cells entered the stationary phase by a process requiring a coupling between its export and immediate extracellular hydrolysis by Ath1p. Compared to what is seen for classical growth conditions on glucose, this mobilization was rather unique, since it took place prior to that of glycogen, which was postponed until the late stationary phase. However, when the Ath1p-dependent mobilization of trehalose identified in this study was impaired, glycogen was mobilized earlier and faster, indicating a fine-tuning control in carbon storage management during periods of carbon and energy restriction.Trehalose is a nonreducing disaccharide of ␣(1,1)-linked glucose present in many organisms, including bacteria, fungi, insects, and plants (12). Fungal cells can accumulate this disaccharide to up to 15% of the cell dry mass depending on growth conditions and environmental stress (for a review, see reference 15). Genetic and metabolic studies led to the proposal that trehalose plays two distinct functions in living cells. On the one hand, it acts as a stress protectant of proteins and biological membranes against adverse conditions (39). On the other hand, it may play a role as a storage carbohydrate in the yeast Saccharomyces cerevisiae. This latter function was suggested by the rapid mobilization of intracellular trehalose upon the resumption of growth of starved cells on a fresh glucose medium and during spore maturation and germination, as well as during oscillatory events in continuous or batch yeast cultures (22,28). Trehalose is also consumed very slowly when cells are maintained in nongrowing conditions, and this breakdown often follows that of glycogen, the major storage carbohydrate in yeast (26, 32), although the mobilization pattern of one glucose store before the other can be dependent on the growth conditions (17, 34, 37).In the yeast S. cerevisiae, the intracellular level of trehalose is the result of a well-regulated balance between enzymatic synthesis and degradation. The synthesis of trehalose is catalyzed by an UDP-glucose-dependent trehalose synthase (TPS) protein complex encoded by four genes. TPS1 and TPS2 encode the trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase, respectively, and TPS3 and TSL1 ...

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Section: Resultsmentioning

confidence: 99%

New Insights into Trehalose Metabolism by Saccharomyces cerevisiae : NTH2 Encodes a Functional Cytosolic Trehalase, and Deletion of TPS1 Reveals Ath1p-Dependent Trehalose Mobilization

Jules

Beltran

François

et al. 2008

Appl Environ Microbiol

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“…For example, it does not only primarily function as a reserve carbohydrate, but also as a highly eYcient protectant, enhancing the resistance of cellular components against adverse conditions such as high temperature, freezing, low dehydration, high osmotic pressure and high concentration of ethanol [7]. It also has been well documented that trehalose has several applications, for example as cryoprotectant for cells in medicine and microbiology, as an eVective component in cosmetics, as a stabilizer for clinical reagents and bioproducts, or even as a preservative for fresh foodstuV [21].…”

Section: Introductionmentioning

confidence: 99%

Trehalose accumulation from corn starch by Saccharomycopsis fibuligera A11 during 2-l fermentation and trehalose purification

Chi

Wang

2009

J Ind Microbiol Biotechnol

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In this study, corn starch was used as the substrate for cell growth and trehalose accumulation by Saccharomycopsis Wbuligera A11. EVect of diVerent aeration rates, agitation speeds, and concentrations of corn starch on direct conversion of corn starch to trehalose by S. Wbuligera A11 were examined using a Biostat B2 2-l fermentor. We found that the optimal conditions for direct conversion of corn starch to trehalose by this yeast strain were that agitation speed was 200 rpm, aeration rate was 4.0 l/min, concentration of corn starch was 2.0% (w/v), initial pH was 5.5, fermentation temperature was 30°C. Under these conditions, over 22.9 g of trehalose per 100 g of cell dry weight was accumulated in the yeast cells, cell mass was 15.2 g/l of the fermentation medium, 0.12% (w/v) of reducing sugar, and 0.21% (w/v) of total sugar were left in the fermented medium within 48 h of the fermentation. It was found that trehalose in the yeast cells could be eYciently extracted by the hot distilled water (80°C). After isolation and puriWcation, the crystal trehalose was obtained from the extract of the cells.

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“…Trehalose is a stress protectant of proteins and cell membranes (1,10,27,33) and is important for the quality and viability of baker's yeast (23,26). The inability to produce trehalose and glycogen before a starvation period results in lower viability (26), and cells whose intracellular trehalose content was increased by the addition of extracellular trehalose had a higher starvation tolerance (23).…”

mentioning

confidence: 99%

“…The inability to produce trehalose and glycogen before a starvation period results in lower viability (26), and cells whose intracellular trehalose content was increased by the addition of extracellular trehalose had a higher starvation tolerance (23).…”

mentioning

confidence: 99%

Starvation Response ofSaccharomyces cerevisiaeGrown in Anaerobic Nitrogen- or Carbon-Limited Chemostat Cultures

Thomsson

Gustafsson

Larsson

2005

Appl Environ Microbiol

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Anaerobic starvation conditions are frequent in industrial fermentation and can affect the performance of the cells. In this study, the anaerobic carbon or nitrogen starvation response of Saccharomyces cerevisiae was investigated for cells grown in anaerobic carbon or nitrogen-limited chemostat cultures at a dilution rate of 0.1 h ؊1 at pH 3.25 or 5. Lactic or benzoic acid was present in the growth medium at different concentrations, resulting in 16 different growth conditions. At steady state, cells were harvested and then starved for either carbon or nitrogen for 24 h under anaerobic conditions. We measured fermentative capacity, glucose uptake capacity, intracellular ATP content, and reserve carbohydrates and found that the carbon, but not the nitrogen, starvation response was dependent upon the previous growth conditions. All cells subjected to nitrogen starvation retained a large portion of their initial fermentative capacity, independently of previous growth conditions. However, nitrogen-limited cells that were starved for carbon lost almost all their fermentative capacity, while carbon-limited cells managed to preserve a larger portion of their fermentative capacity during carbon starvation. There was a positive correlation between the amount of glycogen before carbon starvation and the fermentative capacity and ATP content of the cells after carbon starvation. Fermentative capacity and glucose uptake capacity were not correlated under any of the conditions tested. Thus, the successful adaptation to sudden carbon starvation requires energy and, under anaerobic conditions, fermentable endogenous resources. In an industrial setting, carbon starvation in anaerobic fermentations should be avoided to maintain a productive yeast population.

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Trehalose reserve in Saccharomyces cerevisiae: phenomenon of transport, accumulation and role in cell viability

Cited by 37 publications

References 26 publications

New Insights into Trehalose Metabolism by Saccharomyces cerevisiae : NTH2 Encodes a Functional Cytosolic Trehalase, and Deletion of TPS1 Reveals Ath1p-Dependent Trehalose Mobilization

New Insights into Trehalose Metabolism by Saccharomyces cerevisiae : NTH2 Encodes a Functional Cytosolic Trehalase, and Deletion of TPS1 Reveals Ath1p-Dependent Trehalose Mobilization

Trehalose accumulation from corn starch by Saccharomycopsis fibuligera A11 during 2-l fermentation and trehalose purification

Starvation Response ofSaccharomyces cerevisiaeGrown in Anaerobic Nitrogen- or Carbon-Limited Chemostat Cultures

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