Effects of microcompartmentation on flux distribution and metabolic pools in Chlamydomonas reinhardtii chloroplasts
- Max Planck Institute of Molecular Plant Physiology, Germany
- Carnegie Institution for Science, United States
- Universität Bayreuth, Germany
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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 5 and 6.
Article and author information
Author details
Luke C M Mackinder
Tabea Mettler-Altmann
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
- Daniel J Kliebenstein, University of California, Davis, United States
Version history
- Received: April 30, 2018
- Accepted: September 27, 2018
- Accepted Manuscript published: October 11, 2018 (version 1)
- Version of Record published: November 14, 2018 (version 2)
- Version of Record updated: May 15, 2020 (version 3)
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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Effects of microcompartmentation on flux distribution and metabolic pools in Chlamydomonas reinhardtii chloroplasts
eLife 7:e37960.
https://doi.org/10.7554/eLife.37960
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