Photoprotection and genetic autonomy of plastids in photosynthetic sea slugs

Abstract

Certain sea slugs “steal” the photosynthetic cellular organelles, the plastids, from their prey algae and incorporate them, still functional, inside their own cells. These animals can then remain photosynthetic for months. The redox reactions of photosynthesis are associated with inevitable damage that needs to be constantly repaired. Running photosynthesis with plastids isolated from their algal cell should not be possible, as the algal nucleus that encodes essential maintenance proteins of the photosynthetic machinery is absent in the slug cells. How do photosynthetic sea slugs then avoid or repair the oxidative damage that their plastids should be facing? In my thesis, I have tackled this question by comparing the differences in photosynthetic electron transfer between the photosynthetic sea slug Elysia timida and the source of its plastids, the alga Acetabularia acetabulum. In addition, I compared the rates of photodamage to the plastids in the slugs and in their prey algae. I used the alga Vaucheria litorea, the prey of the slug Elysia chlorotica, to investigate the intrinsic properties of V. litorea plastids that could help explain how these plastids tolerate isolation.

I demonstrate that the slugs maintain the plastoquinone pool of the plastids in an oxidized state in the dark, which can reduce electron pressure and oxidative damage in the photosynthetic electron transfer chain during dark-to-light transitions. The plastids in the slugs also have an increased capacity to dissipate excessive excitation energy as heat compared to the algae. Secondly, I show that most plastids in the slugs are protected against excessive light and UV radiation; tightly packed plastids in the outer layers of the slugs shield the inner ones, and UV radiation is blocked by the slug tissue. Finally, I reveal that the plastids of V. litorea are genetically very autonomous in recovering from photodamage. The relative transcript levels of the plastid encoded translation elongation factor EF-Tu and the plastid maintenance protease FtsH increased in lab-isolated V. litorea plastids during a seven-day incubation period, supporting the view that they likely aid in the longevity of the plastids also inside the slugs. Furthermore, V. litorea plastids produce only low amounts of singlet oxygen, a reactive oxygen species that is known to inhibit the repair machinery of the plastids.