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

Abstract

Background: Some Sacoglossa sea slugs integrate intracellular chloroplasts derived from the algae they feed on, 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 focus our attention on Elysia viridis, a polyphagous species that is mostly found associated to 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 photophysiologic state of the integrated kleptoplasts and the high-performance liquid chromatography (HPLC) to study variations in the photosynthetic pigments. Results: We observed that the photosynthetic efficiency of E. viridis specimens is similar to the one of the respective algal donor but specimens fed with Chaetomorpha tend to have lower performances. Significant differences appear in the non-photochemical quenching (NPQ) abilities. While sea slugs fed with C. tomentosum react to high-light stress as the algae, E. viridis hosting Chaetomorpha chloroplasts are 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.