Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae

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 phosphate...

Descripción completa

Detalles Bibliográficos
Autores principales: Vicente, Rebeca L., Spina, Lucie, Gómez, Jose P.L., Dejean, Sebastien, Parrou, Jean-Luc, François, Jean Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Shared Science Publishers OG 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206404/
https://www.ncbi.nlm.nih.gov/pubmed/30386789
http://dx.doi.org/10.15698/mic2018.10.651
_version_ 1783366358607593472
author Vicente, Rebeca L.
Spina, Lucie
Gómez, Jose P.L.
Dejean, Sebastien
Parrou, Jean-Luc
François, Jean Marie
author_facet Vicente, Rebeca L.
Spina, Lucie
Gómez, Jose P.L.
Dejean, Sebastien
Parrou, Jean-Luc
François, Jean Marie
author_sort Vicente, Rebeca L.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-6206404
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Shared Science Publishers OG
record_format MEDLINE/PubMed
spelling pubmed-62064042018-10-31 Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae Vicente, Rebeca L. Spina, Lucie Gómez, Jose P.L. Dejean, Sebastien Parrou, Jean-Luc François, Jean Marie Microb Cell Microbiology 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. Shared Science Publishers OG 2018-10-01 /pmc/articles/PMC6206404/ /pubmed/30386789 http://dx.doi.org/10.15698/mic2018.10.651 Text en https://creativecommons.org/licenses/by/4.0/ 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 reproduction in any medium, provided the original author and source are acknowledged.
spellingShingle Microbiology
Vicente, Rebeca L.
Spina, Lucie
Gómez, Jose P.L.
Dejean, Sebastien
Parrou, Jean-Luc
François, Jean Marie
Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title_full Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title_fullStr Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title_full_unstemmed Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title_short Trehalose-6-phosphate promotes fermentation and glucose repression in Saccharomyces cerevisiae
title_sort trehalose-6-phosphate promotes fermentation and glucose repression in saccharomyces cerevisiae
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206404/
https://www.ncbi.nlm.nih.gov/pubmed/30386789
http://dx.doi.org/10.15698/mic2018.10.651
work_keys_str_mv AT vicenterebecal trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae
AT spinalucie trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae
AT gomezjosepl trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae
AT dejeansebastien trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae
AT parroujeanluc trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae
AT francoisjeanmarie trehalose6phosphatepromotesfermentationandglucoserepressioninsaccharomycescerevisiae