Control of ATP homeostasis during the respiro‐fermentative transition in yeast

Abstract Respiring Saccharomyces cerevisiae cells respond to a sudden increase in glucose concentration by a pronounced drop of their adenine nucleotide content ([ATP]+[ADP]+[AMP]=[AXP]). The unknown fate of ‘lost’ AXP nucleotides represented a long‐standing problem for the understanding of the yeas...

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Main Authors: Thomas Walther, Maite Novo, Katrin Rössger, Fabien Létisse, Marie‐Odile Loret, Jean‐Charles Portais, Jean‐Marie François
Format: Article
Language:English
Published: Springer Nature 2010-01-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2009.100
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author Thomas Walther
Maite Novo
Katrin Rössger
Fabien Létisse
Marie‐Odile Loret
Jean‐Charles Portais
Jean‐Marie François
author_facet Thomas Walther
Maite Novo
Katrin Rössger
Fabien Létisse
Marie‐Odile Loret
Jean‐Charles Portais
Jean‐Marie François
author_sort Thomas Walther
collection DOAJ
description Abstract Respiring Saccharomyces cerevisiae cells respond to a sudden increase in glucose concentration by a pronounced drop of their adenine nucleotide content ([ATP]+[ADP]+[AMP]=[AXP]). The unknown fate of ‘lost’ AXP nucleotides represented a long‐standing problem for the understanding of the yeast's physiological response to changing growth conditions. Transient accumulation of the purine salvage pathway intermediate, inosine, accounted for the apparent loss of adenine nucleotides. Conversion of AXPs into inosine was facilitated by AMP deaminase, Amd1, and IMP‐specific 5′‐nucleotidase, Isn1. Inosine recycling into the AXP pool was facilitated by purine nucleoside phosphorylase, Pnp1, and joint action of the phosphoribosyltransferases, Hpt1 and Xpt1. Analysis of changes in 24 intracellular metabolite pools during the respiro‐fermentative growth transition in wild‐type, amd1, isn1, and pnp1 strains revealed that only the amd1 mutant exhibited significant deviations from the wild‐type behavior. Moreover, mutants that were blocked in inosine production exhibited delayed growth acceleration after glucose addition. It is proposed that interconversion of adenine nucleotides and inosine facilitates rapid and energy‐cost efficient adaptation of the AXP pool size to changing environmental conditions.
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spelling doaj-art-29595d3f5b1641fa8dfc9964cfed48422025-08-24T12:00:30ZengSpringer NatureMolecular Systems Biology1744-42922010-01-016111710.1038/msb.2009.100Control of ATP homeostasis during the respiro‐fermentative transition in yeastThomas Walther0Maite Novo1Katrin Rössger2Fabien Létisse3Marie‐Odile Loret4Jean‐Charles Portais5Jean‐Marie François6Université de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPUniversité de Toulouse, INSA, UPS, INPAbstract Respiring Saccharomyces cerevisiae cells respond to a sudden increase in glucose concentration by a pronounced drop of their adenine nucleotide content ([ATP]+[ADP]+[AMP]=[AXP]). The unknown fate of ‘lost’ AXP nucleotides represented a long‐standing problem for the understanding of the yeast's physiological response to changing growth conditions. Transient accumulation of the purine salvage pathway intermediate, inosine, accounted for the apparent loss of adenine nucleotides. Conversion of AXPs into inosine was facilitated by AMP deaminase, Amd1, and IMP‐specific 5′‐nucleotidase, Isn1. Inosine recycling into the AXP pool was facilitated by purine nucleoside phosphorylase, Pnp1, and joint action of the phosphoribosyltransferases, Hpt1 and Xpt1. Analysis of changes in 24 intracellular metabolite pools during the respiro‐fermentative growth transition in wild‐type, amd1, isn1, and pnp1 strains revealed that only the amd1 mutant exhibited significant deviations from the wild‐type behavior. Moreover, mutants that were blocked in inosine production exhibited delayed growth acceleration after glucose addition. It is proposed that interconversion of adenine nucleotides and inosine facilitates rapid and energy‐cost efficient adaptation of the AXP pool size to changing environmental conditions.https://doi.org/10.1038/msb.2009.100ATP homeostasismetabolic regulationpurine nucleotide metabolismrespiro‐fermentative transitionyeast
spellingShingle Thomas Walther
Maite Novo
Katrin Rössger
Fabien Létisse
Marie‐Odile Loret
Jean‐Charles Portais
Jean‐Marie François
Control of ATP homeostasis during the respiro‐fermentative transition in yeast
Molecular Systems Biology
ATP homeostasis
metabolic regulation
purine nucleotide metabolism
respiro‐fermentative transition
yeast
title Control of ATP homeostasis during the respiro‐fermentative transition in yeast
title_full Control of ATP homeostasis during the respiro‐fermentative transition in yeast
title_fullStr Control of ATP homeostasis during the respiro‐fermentative transition in yeast
title_full_unstemmed Control of ATP homeostasis during the respiro‐fermentative transition in yeast
title_short Control of ATP homeostasis during the respiro‐fermentative transition in yeast
title_sort control of atp homeostasis during the respiro fermentative transition in yeast
topic ATP homeostasis
metabolic regulation
purine nucleotide metabolism
respiro‐fermentative transition
yeast
url https://doi.org/10.1038/msb.2009.100
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AT maitenovo controlofatphomeostasisduringtherespirofermentativetransitioninyeast
AT katrinrossger controlofatphomeostasisduringtherespirofermentativetransitioninyeast
AT fabienletisse controlofatphomeostasisduringtherespirofermentativetransitioninyeast
AT marieodileloret controlofatphomeostasisduringtherespirofermentativetransitioninyeast
AT jeancharlesportais controlofatphomeostasisduringtherespirofermentativetransitioninyeast
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