• Open Access

Cellular responses of Saccharomyces cerevisiae at near-zero growth rates: transcriptome analysis of anaerobic retentostat cultures

Authors

  • Léonie G.M. Boender,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Antonius J.A. van Maris,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Erik A.F. de Hulster,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Marinka J.H. Almering,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Ida J. van der Klei,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Molecular Cell Biology Group, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Haren, The Netherlands
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  • Marten Veenhuis,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Molecular Cell Biology Group, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Haren, The Netherlands
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  • Johannes H. de Winde,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Jack T. Pronk,

    1. Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
    2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
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  • Pascale Daran-Lapujade

    Corresponding author
    1. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
    • Kluyver Centre for Genomics of Industrial Fermentation, Delft, The Netherlands
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Correspondence: Pascale Daran-Lapujade, Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628 BC Delft, The Netherlands. Tel.: +31 15 2789965; fax: +31 15 2782355; e-mail: p.a.s.daran-lapujade@tudelft.nl

Abstract

Extremely low specific growth rates (below 0.01 h−1) represent a largely unexplored area of microbial physiology. In this study, anaerobic, glucose-limited retentostats were used to analyse physiological and genome-wide transcriptional responses of Saccharomyces cerevisiae to cultivation at near-zero specific growth rates. While quiescence is typically investigated as a result of carbon starvation, cells in retentostat are fed by small, but continuous carbon and energy supply. Yeast cells cultivated near-zero specific growth rates, while metabolically active, exhibited characteristics previously associated with quiescence, including accumulation of storage polymers and an increased expression of genes involved in exit from the cell cycle into G0. Unexpectedly, analysis of transcriptome data from retentostat and chemostat cultures showed, as specific growth rate was decreased, that quiescence-related transcriptional responses were already set in at specific growth rates above 0.025 h−1. These observations stress the need for systematic dissection of physiological responses to slow growth, quiescence, ageing and starvation and indicate that controlled cultivation systems such as retentostats can contribute to this goal. Furthermore, cells in retentostat do not (or hardly) divide while remaining metabolically active, which emulates the physiological status of metazoan post-mitotic cells. We propose retentostat as a powerful cultivation tool to investigate chronological ageing-related processes.

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