1. Biochemistry and Chemical Biology
  2. Plant Biology
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Effects of microcompartmentation on flux distribution and metabolic pools in Chlamydomonas reinhardtii chloroplasts

  1. Anika Küken
  2. Frederik Sommer
  3. Liliya Yaneva-Roder
  4. Luke C M Mackinder
  5. Melanie Höhne
  6. Stefan Geimer
  7. Martin C Jonikas
  8. Michael Schroda
  9. Mark Stitt
  10. Zoran Nikoloski
  11. Tabea Mettler-Altmann  Is a corresponding author
  1. Max Planck Institute of Molecular Plant Physiology, Germany
  2. Carnegie Institution for Science, United States
  3. Universität Bayreuth, Germany
Research Article
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Cite this article as: eLife 2018;7:e37960 doi: 10.7554/eLife.37960

Abstract

Cells and organelles are not homogeneous but include microcompartments that alter the spatiotemporal characteristics of cellular processes. The effects of microcompartmentation on metabolic pathways are however difficult to study experimentally. The pyrenoid is a microcompartment that is essential for a carbon concentrating mechanism (CCM) that improves the photosynthetic performance of eukaryotic algae. Using Chlamydomonas reinhardtii, we obtained experimental data on photosynthesis, metabolites, and proteins in CCM-induced and CCM-suppressed cells. We then employed a computational strategy to estimate how fluxes through the Calvin-Benson cycle are compartmented between the pyrenoid and the stroma. Our model predicts that ribulose-1,5-bisphosphate (RuBP), the substrate of Rubisco, and 3-phosphoglycerate (3PGA), its product, diffuse in and out of the pyrenoid, respectively, with higher fluxes in CCM-induced cells. It also indicates that there is no major diffusional barrier to metabolic flux between the pyrenoid and stroma. Our computational approach represents a stepping stone to understanding microcompartmentalized CCM in other organisms.

Article and author information

Author details

  1. Anika Küken

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1367-0719
  2. Frederik Sommer

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Liliya Yaneva-Roder

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Luke C M Mackinder

    Department of Plant Biology, Carnegie Institution for Science, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1440-3233
  5. Melanie Höhne

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Stefan Geimer

    Institute of Cell Biology, Universität Bayreuth, Bayreuth, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Martin C Jonikas

    Department of Plant Biology, Carnegie Institution for Science, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Schroda

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Mark Stitt

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Zoran Nikoloski

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2671-6763
  11. Tabea Mettler-Altmann

    Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany
    For correspondence
    tabea.mettler@hhu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9161-4889

Funding

Deutsche Forschungsgemeinschaft (EXC 1028)

  • Tabea Mettler-Altmann

Bundesministerium für Bildung und Forschung (FKZ0313924)

  • Frederik Sommer
  • Liliya Yaneva-Roder
  • Michael Schroda
  • Mark Stitt
  • Tabea Mettler-Altmann

Max-Planck-Gesellschaft (Open-access funding)

  • Anika Küken

National Science Foundation (EF-1105617)

  • Martin C Jonikas

National Institutes of Health (DP2-GM-119137)

  • Martin C Jonikas

Simons Foundation (55108535)

  • Martin C Jonikas

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

Reviewing Editor

  1. Daniel J Kliebenstein, University of California, Davis, United States

Publication history

  1. Received: April 30, 2018
  2. Accepted: September 27, 2018
  3. Accepted Manuscript published: October 11, 2018 (version 1)

Copyright

© 2018, Küken 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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