Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus
Type | Article |
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Date | 2024-03 |
Language | English |
Author(s) | Joli Nathalie1, Concia Lorenzo1, Mocaer Karel2, Guterman Julie1, Laude Juliette1, Guerin Sebastien3, Sciandra Theo1, 3, Bruyant Flavienne3, Ait‐mohamed Ouardia1, Beguin Marine3, Forget Marie‐helene3, Bourbousse Clara1, Lacour Thomas4, Bailleul Benjamin5, Nef Charlotte1, Savoie Mireille6, Tremblay Jean‐eric7, Campbell Douglas A.6, Lavaud Johann3, 8, Schwab Yannick9, Babin Marcel3, Bowler Chris1 |
Affiliation(s) | 1 : Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM PSL Université Paris 75005 Paris ,France 2 : Cell Biology and Biophysics Unit European Molecular Biology Laboratory (EMBL) & Collaboration for Joint PhD Degree between the European Molecular Biology Laboratory and the Heidelberg University, Faculty of Biosciences 69117 Heidelberg, Germany 3 : Takuvik International Research Laboratory, Université Laval (Canada) & CNRS (France), Département de Biologie and Québec‐Océan Université Laval Québec QC G1V 0A6 ,Canada 4 : Laboratoire PHYSiologie des micro ALGues (PDG‐ODE‐PHYTOX‐PHYSALG) Centre Atlantique 44 311 Nantes ,France 5 : Laboratory of Chloroplast Biology and Light Sensing in Microalgae, Institut de Biologie Physico Chimique, CNRS Sorbonne Université Paris 75005 ,France 6 : Département de Biologie Université Laval Québec QC G1V 0A6 ,Canada 7 : Mount Allison University Sackville NB E4L 1H3, Canada 8 : UMR 6539 LEMAR‐Laboratory of Environmental Marine Sciences, CNRS/Univ Brest/Ifremer/IRD IUEM‐Institut Européen de la Mer, Technopôle Brest‐Iroise rue Dumont d'Urville 29280 Plouzané ,France 9 : Cell Biology and Biophysics Unit and Electron Microscopy Core Facility European Molecular Biology Laboratory (EMBL) 69117 Heidelberg ,Germany |
Source | New Phytologist (0028-646X) (Wiley), 2024-03 , Vol. 241 , N. 5 , P. 2193-2208 |
DOI | 10.1111/nph.19387 |
Keyword(s) | autophagy, diatom, energy homeostasis, Fragilariopsis cylindrus, polar night, quiescence |
Abstract | Summary Diatoms, the main eukaryotic phytoplankton of the polar marine regions, are essential for the maintenance of food chains specific to Arctic and Antarctic ecosystems, and are experiencing major disturbances under current climate change. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their endurance during the long polar night. Here, using the polar diatom Fragilariopsis cylindrus, we report an integrative analysis combining transcriptomic, microscopic and biochemical approaches to shed light on the strategies used to survive the polar night. We reveal that in prolonged darkness, diatom cells enter a state of quiescence with reduced metabolic and transcriptional activity, during which no cell division occurs. We propose that minimal energy is provided by respiration and degradation of protein, carbohydrate and lipid stores and that homeostasis is maintained by autophagy in prolonged darkness. We also report internal structural changes that manifest the morphological acclimation of cells to darkness, including the appearance of a large vacuole. Our results further show that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis, demonstrating the remarkable robustness of polar diatoms to prolonged darkness at low temperature. |
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