Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
Authors:Rebeca L. Vicente1,2, Lucie Spina1, Jose P.L. Gómez1, Sebastien Dejean3, Jean-Luc Parrou1 and Jean Marie François1,4
doi: 10.15698/mic2018.10.651
Volume 5, pp. 444 to 459, published 01/10/2018.
1 LISBP; UMR INSA-CNRS 5504 & INRA 792; Toulouse, France.
2 Fundación Alfonso Martín Escudero; Madrid, Spain.
3 Institut de Mathématiques de Toulouse, 118 route de Narbonne, F-31062 Toulouse, France.
4 Toulouse White Biotechnology Center, UMS INSA-INRA-CNRS, F-31520 Ramonville.
Keywords:
TPS1, trehalose 6-phosphate, glycolysis, flux sensing, Crabtree effect, glucose repression, Saccharomyces cerevisiae
Corresponding Author(s):
Conflict of interest statement:
The authors declare that they have no competing interests.
Please cite this article as:
Rebeca L. Vicente, Lucie Spina, Jose P.L. Gómez, Sebastien De-jean, Jean-Luc Parrou and Jean Marie François (2018). Trehalose-6-phosphate promotes fermentation and glucose re-pression in Saccharomyces cerevisiae. Microbial Cell 5(10): 444-459. doi: 10.15698/mic2018.10.651
© 2018 Vicente et al. This is an open-access article released under the terms of the Creative Commons Attribution (CC BY) license, which allows the unrestricted use, distribution, and reproduc-tion in any medium, provided the original author and source are acknowledged.
Abstract:
The yeast trehalose-6-phosphate synthase (Tps1) catalyzes the formation of trehalose-6-phosphate (T6P) in trehalose synthesis. Besides, Tps1 plays a key role in carbon and energy homeostasis in this microbial cell, as shown by the well documented loss of ATP and hyper accumulation of sugar phosphates in response to glucose addition in a mutant defective in this protein. The inability of a Saccharomyces cerevisiae tps1 mutant to cope with fermentable sugars is still a matter of debate. We reexamined this question through a quantitative analysis of the capability of TPS1 homologues from different origins to complement phenotypic defects of this mutant. Our results allowed to classify this complementation in three groups. A first group enclosed TPS1 of Klyveromyces lactis with that of S. cerevisiae as their expression in Sctps1 cells fully recovered wild type metabolic patterns and fermentation capacity in response to glucose. At the opposite was the group with TPS1 homologues from the bacteria Escherichia coli and Ralstonia solanacearum, the plant Arabidopsis thaliana and the insect Drosophila melanogaster whose metabolic profiles were comparable to those of a tps1 mutant, notably with almost no accumulation of T6P, strong impairment of ATP recovery and potent reduction of fermentation capacity, albeit these homologous genes were able to rescue growth of Sctps1 on glucose. In between was a group consisting of TPS1 homologues from other yeast species and filamentous fungi characterized by 5 to 10 times lower accumulation of T6P, a weaker recovery of ATP and a 3-times lower fermentation capacity than wild type. Finally, we found that glucose repression of gluconeogenic genes was strongly dependent on T6P. Altogether, our results suggest that the TPS protein is indispensable for growth on fermentable sugars, and points to a critical role of T6P as a sensing molecule that promotes sugar fermentation and glucose repression.