Sacoglossan sea slugs are able to maintain functional chloroplasts inside their own cells, and mechanisms that allow preservation of the chloroplasts are unknown. We found that the slug Elysia timida induces changes to the photosynthetic light reactions of the chloroplasts it steals from the alga Acetabularia acetabulum. Working with a large continuous laboratory culture of both the slugs (>500 individuals) and their prey algae, we show that the plastoquinone pool of slug chloroplasts remains oxidized, which can suppress reactive oxygen species formation. Slug chloroplasts also rapidly build up a strong proton-motive force upon a dark-to-light transition, which helps them to rapidly switch on photoprotective non-photochemical quenching of excitation energy. Finally, our results suggest that chloroplasts inside E. timida rely on oxygen-dependent electron sinks during rapid changes in light intensity. These photoprotective mechanisms are expected to contribute to the long-term functionality of the chloroplasts inside the slugs.
Keywords: Acetabularia acetabulum; Elysia timida; biophysics; cell biology; green algae; kleptoplasty; photosynthetic sea slugs; plant biology.
Plants, algae and a few other organisms rely on a process known as photosynthesis to fuel themselves, as they can harness cellular structures called chloroplasts to convert light into usable energy. Animals typically lack chloroplasts, making them unable to use photosynthesis to power themselves. The sea slug Elysia timida, however, can steal whole chloroplasts from the cells of the algae it consumes: the stolen structures then become part of the cells in the gut of the slug, allowing the animal to gain energy from sunlight. Once they are in the digestive system of the slug, the chloroplasts survive and keep working for longer than expected. Indeed, these structures are often harmed as a side effect of photosynthesis, but the sea slug does not have the right genes to help repair this damage. In addition, conditions inside animal cells are widely different to the ones found inside algae and plants. It is not clear then how the sea slug extends the lifespan of its chloroplasts by preventing damage caused by sunlight. To investigate this question, Havurinne and Tyystjärvi compared photosynthesis in sea slugs and the algae they eat. A range of methods, including measuring fluorescence from the chloroplasts, was used: this revealed that the slug changes the inside of the stolen chloroplasts, making them more resistant to damage. First, when exposed to light the stolen chloroplasts can quickly switch on a mechanism that dissipates light energy to heat, which is less damaging. Second, a molecule that serves as an intermediate during photosynthesis is kept in a ‘safe’ state which prevents it from creating harmful compounds. And finally, additional safeguard molecules ‘deactivate’ compounds that could otherwise mediate damaging reactions. Overall, these measures may reduce the efficiency of the chloroplasts but allow them to keep working for much longer. Early chloroplasts were probably independent bacteria that were captured and ‘domesticated’ by other cells for their ability to extract energy from the sun. Photosynthesizing sea slugs therefore provide an interesting way to understand some of the challenges of early life. The work by Havurinne and Tyystjärvi may also reveal new ways to harness biological processes such as photosynthesis for energy production in other contexts.
© 2020, Havurinne and Tyystjärvi.