The role of trehalose synthesis for the acquisition of thermotolerance in yeast

Abstract

In the yeast Saccharomyces cerevisiae, accumulation of the non-reducing disaccharide trehalose is triggered by various stimuli that activate the heat-schock response. Several studies have shown a close correlation between trehalose levels and tolerance to heat stress, suggesting that trehalose may be a protectant which contributes to thermotolerance. In this study, we have examined mutants defective in genes coding for key enzymes involved in trehalose metabolism with respect to the heat-induced and stationary-phase-induced accumulation of trehalose and the acquisition of thermotolerance. Inactivation of either TPSl or TPS2, encoding subunits of the trehalose-6-phosphate synthase/phosphatase complex, caused an inability to accumulate trehalose upon a mild heat-shock or upon initiation of the stationary phase and significantly reduced the levels of heat-induced and stationary-phase-induced thermotolerance. Deletion of NTHZ, the gene coding for the neutral trehalase, resulted in a defect in trehalose mobilization during recovery from a heat shock which was paralleled by an abnormally slow decrease of thermotolerance. Our results provide strong genetic evidence that heat-induced synthesis of trehalose is an important factor for thermotolerance induction. In an accompanying study [Hottiger, T

Biochemical and genetic characterization of the pathways for trehalose metabolism in Propionibacterium freudenreichii, and their role in stress response

“…The role of trehalose as a scavenger of oxygen radicals has been shown in S. cerevisiae (Benaroudj et al, 2001). On the other hand, the accumulation of trehalose in response to elevated temperature has been reported in several mesophilic organisms, such as yeast, E. coli and Salmonella enterica (Strom & Kaasen, 1993;De Virgilio et al, 1994;Cánovas et al, 2001). Protection against acid stress has not been reported; however, it is interesting that genes for the synthesis of trehalose are present in the genome of Picrophilus torridus, an extreme acidophile with optimal pH for growth of 0.7 (Fütterer et al, 2004).…”

A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis

“…In yeast it is well known that trehalose is involved in heat tolerance (De Virgilio et al 1994;Zentella et al 1999). Here we found that transgenic lines expressing the TPS1-TPS2 gene fusion had a better capacity to tolerate heat stress.…”

“…Trehalose-6-phosphate (T6P) is synthesized from UDP-glucose and glucose-6-phosphate substrates by TPS and dephosphorylated to trehalose by TPP (Cabib and Leloir 1958;Vandercammen et al 1989;Londesborough and Vuorio 1993). Deletion of the TPS1 or TPS2 gene caused an impairment of stress tolerance (Mackenzie et al 1988;De Virgilio et al 1994). Additionally, the yeast tps1 mutant and its alleles are unable to grow in glucose as the sole carbon source.…”

Is thermotolerance of yeast dependent on trehalose accumulation?

“…After preparation of this manuscript we saw a paper of De Virgilio et al [14] which reports experiments with a neutral trehalase deletion mutant with results similar to those described in Table 1 of the present paper. A quantitative difference to our results is that De Virgilio et al found a slow decay of thermotolerance in their trehalase mutant after recovery from heat stress while we do not find any significant difference in the rate of decay of thermotolerance in our wild-type and nthld strain after recovery from heat stress.…”

“…the ability to survive heat shock (lo-20 min treatment at 50-52°C) [14]. This phenomenon is reversible: when the temperature is lowered again to the physiological growth temperature, the trehalose concentration decreases and thermotolerance is reduced [l-3].…”