Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae

Stationary-phase (SP) batch cultures of Saccharomyces cerevisiae, in which growth has been arrested by carbon-source depletion, are widely applied to study chronological lifespan, quiescence and SP-associated robustness. Based on this type of experiments, typically performed under aerobic c...

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Main Authors: Markus M.M. Bisschops, Tim Vos, Rubén Martínez-Moreno, Pilar de la Torre Cortés, Jack T. Pronk, Pascale Daran-Lapujade
Format: Article
Language:English
Published: Shared Science Publishers OG 2015-10-01
Series:Microbial Cell
Subjects:
Online Access:http://microbialcell.com/researcharticles/oxygen-availability-strongly-affects-chronological-lifespan-and-thermotolerance-in-batch-cultures-of-saccharomyces-cerevisiae/
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author Markus M.M. Bisschops
Tim Vos
Rubén Martínez-Moreno
Pilar de la Torre Cortés
Jack T. Pronk
Pascale Daran-Lapujade
author_facet Markus M.M. Bisschops
Tim Vos
Rubén Martínez-Moreno
Pilar de la Torre Cortés
Jack T. Pronk
Pascale Daran-Lapujade
author_sort Markus M.M. Bisschops
collection DOAJ
description Stationary-phase (SP) batch cultures of Saccharomyces cerevisiae, in which growth has been arrested by carbon-source depletion, are widely applied to study chronological lifespan, quiescence and SP-associated robustness. Based on this type of experiments, typically performed under aerobic conditions, several roles of oxygen in aging have been proposed. However, SP in anaerobic yeast cultures has not been investigated in detail. Here, we use the unique capability of S. cerevisiae to grow in the complete absence of oxygen to directly compare SP in aerobic and anaerobic bioreactor cultures. This comparison revealed strong positive effects of oxygen availability on adenylate energy charge, longevity and thermotolerance during SP. A low thermotolerance of anaerobic batch cultures was already evident during the exponential growth phase and, in contrast to the situation in aerobic cultures, was not substantially increased during transition into SP. A combination of physiological and transcriptome analysis showed that the slow post-diauxic growth phase on ethanol, which precedes SP in aerobic, but not in anaerobic cultures, endowed cells with the time and resources needed for inducing longevity and thermotolerance. When combined with literature data on acquisition of longevity and thermotolerance in retentostat cultures, the present study indicates that the fast transition from glucose excess to SP in anaerobic cultures precludes acquisition of longevity and thermotolerance. Moreover, this study demonstrates the importance of a preceding, calorie-restricted conditioning phase in the acquisition of longevity and stress tolerance in SP yeast cultures, irrespective of oxygen availability.
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spelling doaj.art-16f30b037e9a441ea8bea4bda9b7ffff2025-03-12T13:46:44ZengShared Science Publishers OGMicrobial Cell2311-26382015-10-0121142944410.15698/mic2015.11.238123455678Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiaeMarkus M.M. Bisschops0Tim Vos1Rubén Martínez-Moreno2Pilar de la Torre Cortés3Jack T. Pronk4Pascale Daran-Lapujade5Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.Instituto de Ciencias de la Vid y del Vino, CSIC, Universidad de La Rioja, Gobierno de La Rioja, Logroño, Spain.Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.Stationary-phase (SP) batch cultures of Saccharomyces cerevisiae, in which growth has been arrested by carbon-source depletion, are widely applied to study chronological lifespan, quiescence and SP-associated robustness. Based on this type of experiments, typically performed under aerobic conditions, several roles of oxygen in aging have been proposed. However, SP in anaerobic yeast cultures has not been investigated in detail. Here, we use the unique capability of S. cerevisiae to grow in the complete absence of oxygen to directly compare SP in aerobic and anaerobic bioreactor cultures. This comparison revealed strong positive effects of oxygen availability on adenylate energy charge, longevity and thermotolerance during SP. A low thermotolerance of anaerobic batch cultures was already evident during the exponential growth phase and, in contrast to the situation in aerobic cultures, was not substantially increased during transition into SP. A combination of physiological and transcriptome analysis showed that the slow post-diauxic growth phase on ethanol, which precedes SP in aerobic, but not in anaerobic cultures, endowed cells with the time and resources needed for inducing longevity and thermotolerance. When combined with literature data on acquisition of longevity and thermotolerance in retentostat cultures, the present study indicates that the fast transition from glucose excess to SP in anaerobic cultures precludes acquisition of longevity and thermotolerance. Moreover, this study demonstrates the importance of a preceding, calorie-restricted conditioning phase in the acquisition of longevity and stress tolerance in SP yeast cultures, irrespective of oxygen availability.http://microbialcell.com/researcharticles/oxygen-availability-strongly-affects-chronological-lifespan-and-thermotolerance-in-batch-cultures-of-saccharomyces-cerevisiae/chronological lifespanthermotolerancestationary phaseanaerobiosisenergeticstranscriptional responseconditioning
spellingShingle Markus M.M. Bisschops
Tim Vos
Rubén Martínez-Moreno
Pilar de la Torre Cortés
Jack T. Pronk
Pascale Daran-Lapujade
Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
Microbial Cell
chronological lifespan
thermotolerance
stationary phase
anaerobiosis
energetics
transcriptional response
conditioning
title Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
title_full Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
title_fullStr Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
title_full_unstemmed Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
title_short Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae
title_sort oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of saccharomyces cerevisiae
topic chronological lifespan
thermotolerance
stationary phase
anaerobiosis
energetics
transcriptional response
conditioning
url http://microbialcell.com/researcharticles/oxygen-availability-strongly-affects-chronological-lifespan-and-thermotolerance-in-batch-cultures-of-saccharomyces-cerevisiae/
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