Food shaped photosynthesis: Photophysiology of the sea slug Elysia viridis fed with two alternative chloroplast donors

Open Res Eur. 2024 Mar 13:3:107. doi: 10.12688/openreseurope.16162.2. eCollection 2023.

Abstract

Background: Some Sacoglossa sea slugs steal and integrate chloroplasts derived from the algae they feed on into their cells where they continue to function photosynthetically, a process termed kleptoplasty. The stolen chloroplasts - kleptoplasts - can maintain their functionality up to several months and support animal metabolism. However, chloroplast longevity can vary depending on sea slug species and algal donor. In this study, we focused on Elysia viridis, a polyphagous species that is mostly found associated with the macroalga Codium tomentosum, but that was reported to eat other macroalgae, including Chaetomorpha sp.

Methods: We have investigated the changes in E. viridis physiology when provided with the two different food sources to evaluate to which extent the photosynthetic and photoprotective mechanisms of the algae chloroplasts matched those of the plastids once in the animal cells. To perform the study, we rely on the evaluation of chlorophyll a variable fluorescence to study the photophysiological state of the integrated kleptoplasts and high-performance liquid chromatography (HPLC) to study variations in the photosynthetic pigments.

Results: We observed that the photosynthetic efficiency of E. viridis is lower when fed with Chaetomorpha. Also, significant differences were observed in the non-photochemical quenching (NPQ) abilities of the sea slugs. While sea slugs fed with C. tomentosum react similarly to high-light stress as the alga, E. viridis hosting Chaetomorpha chloroplasts were unable to properly recover from photoinhibition or perform a functional xanthophyll cycle (XC).

Conclusions: Our results showed that, even if the sea slugs fed with the two algae show photosynthetic activities like the respective algal donors, not all the photoprotective mechanisms present in Chaetomorpha can be maintained in E. viridis. This indicates that the functionality of the kleptoplasts does not depend solely on their origin but also on the degree of compatibility with the animal species integrating them.

Keywords: Kleptoplasty; NPQ; Sacoglossa; photoprotection; xanthophyll cycle..

Plain language summary

Sea slugs known as Sacoglossa (also called "solar-powered sea slugs") have a fascinating ability to steal and use chloroplasts from the algae they eat. This process is called kleptoplasty. These stolen chloroplasts, also called kleptoplasts, can remain functional for several months and help the sea slugs with their metabolism by performing photosynthesis like plants. However, the time of chloroplast maintenance can vary depending on the species of sea slug and the type of algae they feed on. In this study, we focused on a species called Elysia viridis, which eats various types of algae, including Codium tomentosum and Chaetomorpha sp. These two algae have different characteristics when it comes to photosynthesis and protection against excessive light. We investigated how the physiology of E. viridis changed when it was given these two different food sources. Our results show that sea slugs had similar photosynthetic activities to their respective food alga. However, not all photoprotective mechanisms of Chaetomorpha algae could be maintained in E. viridis. This suggests that the functionality of the stolen chloroplasts depends not only on their source but also on how well they match the sea slug species that incorporate them.

Grants and funding

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 949880) (S.C.), and by Fundação para a Ciência e a Tecnologia, grants no. 2020.03278 CEECIND (S.C.), CEECIND/01434/2018 (P.C.), and UIDB/50017/2020+UIDP/50017/2020 (CESAM).