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.

寄生虫在海洋浮游生物中分布广泛且种类繁多，其中许多寄生虫感染单细胞藻类以求生存。这些寄生虫如何在宿主体内发育和清除能量，以及宿主的细胞组织和新陈代谢如何改变，仍然是悬而未决的问题。将定量结构和化学成像与时间分辨转录组学相结合，我们揭示了海洋寄生虫变形虫的显着形态和代谢变化（Syndiniales）在细胞内感染期间，特别是在吞噬和消化富含营养的宿主染色体之后。变化包括体积增加 200 倍的顺序无嵴和​​嵴状线粒体、核体积增加 13 倍、高尔基体的发育以及从糖酵解（在宿主内）到 TCA（自由生存的恐龙孢子）的代谢转换。在顶复门寄生虫中观察到类似的变化，从而强调了由代谢限制和感染周期驱动的趋同性状。在藻类宿主中，产生能量的细胞器（质体、线粒体）在大部分感染期间保持相对完整。我们还观察到糖储备减少，而脂滴增加。快速感染宿主细胞核可能是一种“僵尸化”策略，