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

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.