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

Authors:

Markus M.M. Bisschops1,3,#, Tim Vos1,#, Rubén Martínez-Moreno2,4, Pilar de la Torre Cortés1, Jack T. Pronk1, Pascale Daran-Lapujade1

doi: 10.15698/mic2015.11.238
Volume 2, pp. 429 to 444, published 21/10/2015.

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Affiliations:

1 Department of Biotechnology, Delft University of Technology, Delft, The Netherlands.

2 Instituto de Ciencias de la Vid y del Vino, CSIC, Universidad de La Rioja, Gobierno de La Rioja, Logroño, Spain.

3 Current address: Division of Systems and Synthetic Biology, Department of Biology and Biological Engineering & The Novo Nordisk Foundation Center for Biosustainability, Chalmers University of Technology, Gothenburg, Sweden.

4 Current address: Quercus Europe S.L., L’Hospitalet de Llobregat, Catalonia, Spain.

# Authors contributed equally to this work.

Keywords: 

chronological lifespan, thermotolerance, stationary phase, anaerobiosis, energetics, transcriptional response, conditioning

Corresponding Author(s):

Pascale Daran-Lapujade, Julianalaan 67, 2628 BC; Delft, The Netherlands p.a.s.daran-lapujade@tudelft.nl

Conflict of interest statement:

The authors declare no conflict of interest.

Please cite this article as:

Markus M.M. Bisschops, Tim Vos, Rubén Martínez-Moreno, Pilar de la Torre Cortes, Jack T. Pronk, Pascale Daran-Lapujade (2015). Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae. Microbial Cell2(11): 429-444.

© 2015 Bisschops 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 reproduction in any medium, provided the original author and source are acknowledged.

Abstract:

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.