A wide spectrum of biological interactions shapes today’s aquatic ecosystems. Within plankton, predators, parasites, primary producers, and viruses structure food webs and drive biogeochemical cycles. Some heterotrophic eukaryotes acquire photosynthetic capacity from microalgae via photosymbiosis, where whole algae are retained, or kleptoplasty, where only plastids are sequestered, for periods ranging from a few hours to several months. These associations offer insights into the evolutionary history of plastid acquisition in eukaryotes, yet the cellular mechanisms that sustain them remain poorly understood. In particular, kleptoplasty is an intriguing process whereby plastids are no longer sustained and controlled by their nucleus. This raises the central question: how do these “orphan” plastids remain functional and beneficial within a foreign host over time? This PhD thesis investigates a kleptoplastic dinoflagellate from the Ross Sea (RSD), which steals and retains plastids from the microalga Phaeocystis antarctica for several months.
Chapter I establishes the baseline state of ingested organelles under constant feeding (presence of algal prey). 3D Electron microscopy and photophysiology show that RSD acquires not only plastids but also algal nuclei and mitochondria. Compared to the free-living microalga, plastids and pyrenoids increase in volume inside the host, and photosynthetic activity such oxygen production is enhanced, temporarily supported by a large algal nucleus that persists for about a week.
​Chapter II examines the fate of algal organelles during starvation (absence of algal prey source). Ultrastructural imaging, NanoSIMS isotope labelling, photophysiology, and transcriptomic analysis show that plastids remain functional for over two months even after the loss of the nucleus. Carbon fixation and transfer to the host is observed, and mitochondria reorganise into networks closely interacting with plastids. The fact that plastids and mitochondria remain functional in the host for months, even without the algal nucleus, raises new questions about host control and organelle cross-talk.
Chapter III compares fed and starved host cells to better understand the molecular mechanisms underlying plastid maintenance. Proteomics, Western blots, and Ultrastructure Expansion Microscopy (U-ExM) show that nuclear-encoded proteins (e.g. photosystems) persist in plastids after several weeks of starvation. Proteomic analysis further indicates that most proteins required for plastid and mitochondrial function remain detectable in nine-week starved samples despite the absence of the nucleus. However, further proteomic analysis on isolated stolen plastids or host cells under different light or stress conditions will be needed to determine whether these proteins are stably retained over time or supplied by the host.
The thesis concludes by exploring RSD’s biogeographic distribution and prey specificity better to understand the ecology and functioning of polar kleptoplasty. Studying these transient associations provides snapshots of early endosymbiotic events while revealing their role in plankton ecology and nutrient cycling. Overall, this work opens new avenues in the field of kleptoplasty and raises fundamental questions on the evolutionary trajectory of such cellular interactions. ​​​​​
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​ Keywords
​Photosynthesis, Marine plankton, Kleptoplastidy, 3D electron microscopy, Photophysiology