Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus
International audience 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 und...
Published in: | New Phytologist |
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Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2023
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Subjects: | |
Online Access: | https://hal.science/hal-04357816 https://hal.science/hal-04357816/document https://hal.science/hal-04357816/file/2023f-NewPhytologist.pdf https://doi.org/10.1111/nph.19387 |
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ftunivaixmarseil:oai:HAL:hal-04357816v1 |
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record_format |
openpolar |
institution |
Open Polar |
collection |
Aix-Marseille Université: HAL |
op_collection_id |
ftunivaixmarseil |
language |
English |
topic |
quiescence autophagy diatom energy homeostasis Fragilariopsis cylindrus polar night [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology |
spellingShingle |
quiescence autophagy diatom energy homeostasis Fragilariopsis cylindrus polar night [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology Joli, Nathalie Concia, Lorenzo Mocaer, Karel Guterman, Julie Laude, Juliette Guerin, Sebastien Sciandra, Theo Bruyant, Flavienne Ait‐mohamed, Ouardia Beguin, Marine Forget, Marie‐helene Richet-Bourbousse, Clara Lacour, Thomas Bailleul, Benjamin Nef, Charlotte Savoie, Mireille Tremblay, Jean‐eric Campbell, Douglas, A Lavaud, Johann Schwab, Yannick Babin, Marcel Bowler, Chris Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
topic_facet |
quiescence autophagy diatom energy homeostasis Fragilariopsis cylindrus polar night [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology |
description |
International audience 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. |
author2 |
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) EMBL Heidelberg Takuvik International Research Laboratory Université Laval Québec (ULaval)-Centre National de la Recherche Scientifique (CNRS) Unité Physiologie et Toxines des Microalgues Toxiques et Nuisibles (PHYTOX) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut de biologie physico-chimique (IBPC (FR_550)) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) Université Laval Québec (ULaval) Mount Allison University Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE) Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN) Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili |
format |
Article in Journal/Newspaper |
author |
Joli, Nathalie Concia, Lorenzo Mocaer, Karel Guterman, Julie Laude, Juliette Guerin, Sebastien Sciandra, Theo Bruyant, Flavienne Ait‐mohamed, Ouardia Beguin, Marine Forget, Marie‐helene Richet-Bourbousse, Clara Lacour, Thomas Bailleul, Benjamin Nef, Charlotte Savoie, Mireille Tremblay, Jean‐eric Campbell, Douglas, A Lavaud, Johann Schwab, Yannick Babin, Marcel Bowler, Chris |
author_facet |
Joli, Nathalie Concia, Lorenzo Mocaer, Karel Guterman, Julie Laude, Juliette Guerin, Sebastien Sciandra, Theo Bruyant, Flavienne Ait‐mohamed, Ouardia Beguin, Marine Forget, Marie‐helene Richet-Bourbousse, Clara Lacour, Thomas Bailleul, Benjamin Nef, Charlotte Savoie, Mireille Tremblay, Jean‐eric Campbell, Douglas, A Lavaud, Johann Schwab, Yannick Babin, Marcel Bowler, Chris |
author_sort |
Joli, Nathalie |
title |
Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
title_short |
Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
title_full |
Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
title_fullStr |
Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
title_full_unstemmed |
Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus |
title_sort |
hypometabolism to survive the long polar night and subsequent successful return to light in the diatom fragilariopsis cylindrus |
publisher |
HAL CCSD |
publishDate |
2023 |
url |
https://hal.science/hal-04357816 https://hal.science/hal-04357816/document https://hal.science/hal-04357816/file/2023f-NewPhytologist.pdf https://doi.org/10.1111/nph.19387 |
genre |
Antarc* Antarctic Arctic Climate change Phytoplankton polar night |
genre_facet |
Antarc* Antarctic Arctic Climate change Phytoplankton polar night |
op_source |
ISSN: 0028-646X EISSN: 1469-8137 New Phytologist https://hal.science/hal-04357816 New Phytologist, 2023, 241 (5), pp.2193-2208. ⟨10.1111/nph.19387⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1111/nph.19387 hal-04357816 https://hal.science/hal-04357816 https://hal.science/hal-04357816/document https://hal.science/hal-04357816/file/2023f-NewPhytologist.pdf doi:10.1111/nph.19387 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1111/nph.19387 |
container_title |
New Phytologist |
_version_ |
1799477079848255488 |
spelling |
ftunivaixmarseil:oai:HAL:hal-04357816v1 2024-05-19T07:29:01+00:00 Hypometabolism to survive the long polar night and subsequent successful return to light in the diatom Fragilariopsis cylindrus Joli, Nathalie Concia, Lorenzo Mocaer, Karel Guterman, Julie Laude, Juliette Guerin, Sebastien Sciandra, Theo Bruyant, Flavienne Ait‐mohamed, Ouardia Beguin, Marine Forget, Marie‐helene Richet-Bourbousse, Clara Lacour, Thomas Bailleul, Benjamin Nef, Charlotte Savoie, Mireille Tremblay, Jean‐eric Campbell, Douglas, A Lavaud, Johann Schwab, Yannick Babin, Marcel Bowler, Chris 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) EMBL Heidelberg Takuvik International Research Laboratory Université Laval Québec (ULaval)-Centre National de la Recherche Scientifique (CNRS) Unité Physiologie et Toxines des Microalgues Toxiques et Nuisibles (PHYTOX) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut de biologie physico-chimique (IBPC (FR_550)) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) Université Laval Québec (ULaval) Mount Allison University Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE) Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN) Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili 2023-12-14 https://hal.science/hal-04357816 https://hal.science/hal-04357816/document https://hal.science/hal-04357816/file/2023f-NewPhytologist.pdf https://doi.org/10.1111/nph.19387 en eng HAL CCSD Wiley info:eu-repo/semantics/altIdentifier/doi/10.1111/nph.19387 hal-04357816 https://hal.science/hal-04357816 https://hal.science/hal-04357816/document https://hal.science/hal-04357816/file/2023f-NewPhytologist.pdf doi:10.1111/nph.19387 info:eu-repo/semantics/OpenAccess ISSN: 0028-646X EISSN: 1469-8137 New Phytologist https://hal.science/hal-04357816 New Phytologist, 2023, 241 (5), pp.2193-2208. ⟨10.1111/nph.19387⟩ quiescence autophagy diatom energy homeostasis Fragilariopsis cylindrus polar night [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology info:eu-repo/semantics/article Journal articles 2023 ftunivaixmarseil https://doi.org/10.1111/nph.19387 2024-04-25T00:38:00Z International audience 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. Article in Journal/Newspaper Antarc* Antarctic Arctic Climate change Phytoplankton polar night Aix-Marseille Université: HAL New Phytologist |