Parasites are widespread and diverse in oceanic plankton and many of them infect single-celled algae for survival. How these parasites develop and scavenge energy within the host and how the cellular organization and metabolism of the host is altered remain open questions. Combining quantitative structural and chemical imaging with time-resolved transcriptomics, we unveil dramatic morphological and metabolic changes of the marine parasite Amoebophrya (Syndiniales) during intracellular infection, particularly following engulfment and digestion of nutrient-rich host chromosomes. Changes include a sequential acristate and cristate mitochondrion with a 200-fold increase in volume, a 13-fold increase in nucleus volume, development of Golgi apparatus and a metabolic switch from glycolysis (within the host) to TCA (free-living dinospore). Similar changes are seen in apicomplexan parasites, thus underlining convergent traits driven by metabolic constraints and the infection cycle. In the algal host, energy-producing organelles (plastid, mitochondria) remain relatively intact during most of the infection. We also observed that sugar reserves diminish while lipid droplets increase. Rapid infection of the host nucleus could be a "zombifying" strategy, allowing the parasite to digest nutrient-rich chromosomes and escape cytoplasmic defense, whilst benefiting from maintained carbon-energy production of the host cell.

Cell Biology and Biophysics Unit European Molecular Biology Laboratory 69117 Heidelberg Germany

Institut de Biologie Structurale University Grenoble Alpes CEA CNRS 38044 Grenoble France

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Laboratoire de Biologie des Organismes et Ecosystèmes Aquatiques Université de Caen Normandie MNHN SU UA CNRS UMR 8067 IRD 207 14000 Caen France

Laboratoire Physiologie Cellulaire et Végétale Univ Grenoble Alpes CNRS CEA INRAE IRIG DBSCI LPCV 38000 Grenoble France

Ramaciotti Centre for Cryo Electron Microscopy Monash University Clayton 3800 VIC Australia

Sorbonne Université CNRS UMR7144 Adaptation et Diversité en Milieu Marin Ecology of Marine Plankton Station Biologique de Roscoff 29680 Roscoff France

The Centre for Microscopy Characterisation and Analysis The University of Western Australia Perth WA 6009 Australia

Université François Rabelais Laboratoire Biologie cellulaire et Microscopie électronique 37032 Tours France

UWA School of Biological Sciences The University of Western Australia Perth WA 6009 Australia

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