Hypometabolism to survive the long polar night in the diatom Fragilariopsis cylindrus

• Main Authors: Joli, Nathalie, Concia, Lorenzo, Mocaer, Karel, Guterman, Julie, Laude, Juliette, Guerin, Sebastien, Sciandra, Theo, Bruyant, Flavienne, Ait-Mohamed, Ouardia, Beguin, Marine, Forget, Marie-Helene, Bourbousse, Clara, Lacour, Thomas, Bailleul, Benjamin, Tremblay, Jean-Eric, Campbell, Douglas, Lavaud, Johan, Schwab, Yannick, Babin, Marcel, Bowler, Chris
• Other Authors: Institut de biologie de l'ENS Paris (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de biologie physico-chimique (IBPC (FR_550)), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)
• Format: Report
• Language: English
• Published: HAL CCSD 2023
• Subjects: [SDV]Life Sciences [q-bio]; Arctic; Antarctic; Antarc*; Phytoplankton; polar night
• Online Access: https://hal.science/hal-04268690; https://doi.org/10.1101/2023.01.14.524047

Abstract Diatoms, the major eukaryotic phytoplankton in polar regions, are essential to sustain Arctic and Antarctic ecosystems. As such, it is fundamental to understand the physiological mechanisms and associated molecular basis of their resilience to the long polar night. Here, we report an integrative approach revealing that in prolonged darkness, diatom cells enter a state of quiescence associated 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. Our results further indicate that immediately following a return to light, diatom cells are able to use photoprotective mechanisms and rapidly resume photosynthesis. Cell division resumed rates similar to those before darkness. Our study demonstrates the remarkable robustness of polar diatoms to prolonged darkness at low temperatures. Graphical abstract Teaser To survive the long winter, polar diatoms slow down metabolism and express genes to assure survival following return to light.