Morphological bases of phytoplankton energy management and physiological responses unveiled by 3D subcellular imaging

Clarisse Uwizeye, Johan Decelle (), Pierre-Henri Jouneau, Serena Flori, Benoit Gallet, Jean-Baptiste Keck, Davide Dal Bo, Christine Moriscot, Claire Seydoux, Fabien Chevalier, Nicole L. Schieber, Rachel Templin, Guillaume Allorent, Florence Courtois, Gilles Curien, Yannick Schwab, Guy Schoehn, Samuel C. Zeeman, Denis Falconet () and Giovanni Finazzi ()
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Clarisse Uwizeye: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Johan Decelle: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Pierre-Henri Jouneau: Univ. Grenoble Alpes, CEA, IRIG-MEM
Serena Flori: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Benoit Gallet: Univ. Grenoble Alpes, CNRS, CEA, IRIG-IBS
Jean-Baptiste Keck: Univ. Grenoble Alpes, Laboratoire Jean Kuntzmann
Davide Dal Bo: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Christine Moriscot: Univ. Grenoble Alpes, CNRS, CEA, IRIG-IBS
Claire Seydoux: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Fabien Chevalier: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Nicole L. Schieber: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory
Rachel Templin: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory
Guillaume Allorent: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Florence Courtois: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Gilles Curien: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Yannick Schwab: Cell Biology and Biophysics Unit, European Molecular Biology Laboratory
Guy Schoehn: Univ. Grenoble Alpes, CNRS, CEA, IRIG-IBS
Samuel C. Zeeman: ETH Zurich
Denis Falconet: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV
Giovanni Finazzi: Univ. Grenoble Alpes, CNRS, CEA, INRAe, IRIG-LPCV

Nature Communications, 2021, vol. 12, issue 1, 1-12

Abstract: Abstract Eukaryotic phytoplankton have a small global biomass but play major roles in primary production and climate. Despite improved understanding of phytoplankton diversity and evolution, we largely ignore the cellular bases of their environmental plasticity. By comparative 3D morphometric analysis across seven distant phytoplankton taxa, we observe constant volume occupancy by the main organelles and preserved volumetric ratios between plastids and mitochondria. We hypothesise that phytoplankton subcellular topology is modulated by energy-management constraints. Consistent with this, shifting the diatom Phaeodactylum from low to high light enhances photosynthesis and respiration, increases cell-volume occupancy by mitochondria and the plastid CO2-fixing pyrenoid, and boosts plastid-mitochondria contacts. Changes in organelle architectures and interactions also accompany Nannochloropsis acclimation to different trophic lifestyles, along with respiratory and photosynthetic responses. By revealing evolutionarily-conserved topologies of energy-managing organelles, and their role in phytoplankton acclimation, this work deciphers phytoplankton responses at subcellular scales.

Date: 2021
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DOI: 10.1038/s41467-021-21314-0

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