Abstract

Cells constantly adapt to environmental fluctuations. These physiological changes require time and therefore cause a lag phase during which the cells do not function optimally. Interestingly, past exposure to an environmental condition can shorten the time needed to adapt when the condition re-occurs, even in daughter cells that never directly encountered the initial condition. Here, we use the molecular toolbox of Saccharomyces cerevisiae to systematically unravel the molecular mechanism underlying such history-dependent behavior in transitions between glucose and maltose. In contrast to previous hypotheses, the behavior does not depend on persistence of proteins involved in metabolism of a specific sugar. Instead, presence of glucose induces a gradual decline in the cells' ability to activate respiration, which is needed to metabolize alternative carbon sources. These results reveal how trans-generational transitions in central carbon metabolism generate history-dependent behavior in yeast, and provide a mechanistic framework for similar phenomena in other cell types.

Data availability

The RNA-seq and BAR-seq data-sets are deposited in GEO. The GEO accession number of BAR-Seq and RNA-Seq data are GSE116505 and GSE116246 respectively.

The following data sets were generated
    1. Cerulus B
    2. Jariani A
    (2018) BAR-Seq to study history-dependent behavior
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE116505).

Article and author information

Author details

  1. Bram Cerulus

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  2. Abbas Jariani

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  3. Gemma Perez-Samper

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  4. Lieselotte Vermeersch

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5789-2220
  5. Julian M J Pietsch

    Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9992-2384
  6. Matthew M Crane

    Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
  7. Aaron M New

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  8. Brigida Gallone

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  9. Miguel Roncoroni

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    Miguel Roncoroni, This author had substantial contributions to acquisition of data and doing the experiments.
  10. Maria C Dzialo

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  11. Sander K Govers

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0260-4054
  12. Jhana Hendrickx

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  13. Eva Galle

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  14. Maarten Coomans

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  15. Pieter Berden

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  16. Sara Verbandt

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    Competing interests
    No competing interests declared.
  17. Peter S Swain

    Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7489-8587
  18. Kevin J Verstrepen

    VIB Laboratory for Systems Biology, VIB-KU Leuven Center for Microbiology, Leuven, Belgium
    For correspondence
    kevin.verstrepen@kuleuven.vib.be
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3077-6219

Funding

Fonds Wetenschappelijk Onderzoek

  • Bram Cerulus
  • Lieselotte Vermeersch

Vlaams Instituut voor Biotechnologie

  • Kevin J Verstrepen

European Research Counsil (CoG682009)

  • Bram Cerulus
  • Abbas Jariani
  • Gemma Perez-Samper
  • Kevin J Verstrepen

Agentschap Innoveren & Ondernemen

  • Kevin J Verstrepen

AB-InBev-Baillet Latour Fund

  • Kevin J Verstrepen

Human Frontier Science Program (246 RGP0050/2013)

  • Abbas Jariani
  • Peter S Swain
  • Kevin J Verstrepen

SULSA Postdoctoral Exchange Scheme

  • Julian M J Pietsch

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Version history

  1. Received: June 19, 2018
  2. Accepted: October 5, 2018
  3. Accepted Manuscript published: October 9, 2018 (version 1)
  4. Version of Record published: November 1, 2018 (version 2)

Copyright

© 2018, Cerulus et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Bram Cerulus
  2. Abbas Jariani
  3. Gemma Perez-Samper
  4. Lieselotte Vermeersch
  5. Julian M J Pietsch
  6. Matthew M Crane
  7. Aaron M New
  8. Brigida Gallone
  9. Miguel Roncoroni
  10. Maria C Dzialo
  11. Sander K Govers
  12. Jhana Hendrickx
  13. Eva Galle
  14. Maarten Coomans
  15. Pieter Berden
  16. Sara Verbandt
  17. Peter S Swain
  18. Kevin J Verstrepen
(2018)
Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources
eLife 7:e39234.
https://doi.org/10.7554/eLife.39234

Share this article

https://doi.org/10.7554/eLife.39234

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