Hijacking and integration of algal plastids and mitochondria in a polar planktonic host

作     者：Rao, Ananya Kedige Yee, Daniel Chevalier, Fabien LeKieffre, Charlotte Pavie, Marie Olivetta, Marine Dudin, Omaya Gallet, Benoit Hehenberger, Elisabeth Seifi, Mehdi Jug, Florian Deschamps, Joran Wu, Ting-Di Gast, Rebecca Jouneau, Pierre-Henri Decelle, Johan 

作者机构：Cell and Plant Physiology Laboratory CNRS CEA INRAE IRIG Université Grenoble Alpes Grenoble 38054 France Department of Biochemistry Université de Genève Genève 1211 Switzerland Université Grenoble Alpes CEA CNRS IBS Grenoble 38000 France Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice 37005 Czech Republic Computational Biology Research Centre Human Technopole Milan 20157 Italy Bioimage Analysis Unit National Facility for Data Handling and Analysis Human Technopole Milan 20157 Italy Institut Curie PSL University University of Paris-Saclay CNRS UAR2016 Inserm US43 Multimodal Imaging Center Orsay 91400 France Woods Hole Oceanographic Institution Woods Hole 02543 MA United States University Grenoble Alpes CEA IRIG-MEM Grenoble 38054 France 

出 版 物：《Current Biology》 (Curr. Biol.)

年 卷 期：2025年第35卷第11期

页      面：2509-2523.e7页

学科分类：0710[理学-生物学] 07[理学] 09[农学] 

基　　金：Agence Nationale de la Recherche, ANR Plant and Cell Physiology laboratory Grenoble Instruct-ERIC center Université de Genève, UNIGE AI4Life Horizon Europe Program Consortium European Commission, EU Région Auvergne-Rhône-Alpes Fondation pour la Recherche Médicale, FRM Infrastructures en Biologie Santé et Agronomie, IBiSA European Regional Development Fund, ERDF BioGenouest network Gordon and Betty Moore Foundation, GBMF French Infrastructure for Integrated Structural Biology, FRISBI, (ANR-10-INBS-05-02, ANR-17-EURE-0003) French Infrastructure for Integrated Structural Biology, FRISBI ISBG, (UMS 3518 CNRS-CEA-UGAEMBL) HORIZON EUROPE Framework Programme, (101057970-AI4LIFE) HORIZON EUROPE Framework Programme Akademie Věd České Republiky, CAS, (LQ200962204) Akademie Věd České Republiky, CAS ANR EPHEMER, (ANR-21-CE02-0030) Institut Curie, (ANR-22-PEEL-0014) Institut Curie European Research Council, ERC, (101088661) European Research Council, ERC Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, SNF, (TMSGI3_218007) Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, SNF Institut Français de Bioinformatique, IFB, (ANR-11-INBS-0013) Institut Français de Bioinformatique, IFB 

主　　题：3D electron microscopy dinoflagellate kleptoplastidy marine plankton microalga mitochondria photosynthesis plastid symbiosis 

摘      要：In oceanic plankton, various hosts are capable of engulfing and temporarily integrating microalgae (photosymbiosis) or just their photosynthetic plastids (kleptoplastidy) from the environment. These cellular interactions have been hypothesized to be representative of evolutionary steps in plastid acquisition in eukaryotes, but the underlying mechanisms are not fully understood. Here, we studied a polar kleptoplastidic dinoflagellate, which is known to steal plastids of the microalga Phaeocystis antarctica. We tracked the morphology and activity of stolen plastids over several months by combining multimodal subcellular imaging and photophysiology. Upon integration inside a host vacuole, the volume of plastids and pyrenoids significantly increased, and photosynthetic activity was boosted. This may be supported by the retention of a 50-fold larger algal nucleus for ∼1 week. Once the algal nucleus was lost, there was a decrease in plastid volume and photosynthesis, but nucleus- and plastid-encoded photosystem subunits were still detected. Carbon fixation and transfer to the host were also maintained after 2 months. We also showed that the algal mitochondrion was stolen and retained for several months, transforming into an extensive network interacting with plastids. This highlights a complex strategy in plankton along the continuum of plastid symbioses, where both plastids and mitochondria of a microalga are hijacked by a host for several months without the algal nucleus. This association, which we found to be widely distributed in polar regions, suggests that plastid-mitochondrion interaction may have played a role in the evolution of plastid acquisition and opens new questions about host control and organelle maintenance. © 2025 The Authors