Photosynthesis from stolen chloroplasts can support sea slug reproductive fitness

Abstract

Some sea slugs are able to steal functional chloroplasts (kleptoplasts) from their algal food sources, but the role and relevance of photosynthesis to the animal host remain controversial. While some researchers claim that kleptoplasts are slowly digestible ‘snacks’, others advocate that they enhance the overall fitness of sea slugs much more profoundly. Our analysis shows light-dependent incorporation of 13 C and 15 N in the albumen gland and gonadal follicles of the sea slug Elysia timida , representing translocation of photosynthates to kleptoplast-free reproductive organs. Long-chain polyunsaturated fatty acids with reported roles in reproduction were produced in the sea slug cells using labelled precursors translocated from the kleptoplasts. Finally, we report reduced fecundity of E. timida by limiting kleptoplast photosynthesis. The present study indicates that photosynthesis enhances the reproductive fitness of kleptoplast-bearing sea slugs, confirming the biological relevance of this remarkable association between a metazoan and an algal-derived organelle.

Pigment and Fatty Acid Heterogeneity in the Sea Slug Elysia crispata Is Not Shaped by Habitat Depth

“…This could be due to the larger size of E. crispata , when compared to E. viridis and P. dendritica , as well as the foliose shape of its parapodia, hence allowing E. crispata to harbour a higher number of kleptoplasts in proportion to its body size. Analyses of lipids and FAs, as performed before for E. chlorotica, E. viridis and E. timida , could be important for estimating kleptoplast energetic contribution for the animal and their specific support in reproductive fitness [ 33 , 36 , 48 , 59 ]. To understand if something similar occurs in E. crispata , further studies using isotope labeling are still required [ 36 ].…”

“…The lack of DHA in E. crispata samples may be related to the absence of this FA in its food sources. Although this is a common FA in marine organisms, it is absent in macroalgae recognized as common food sources of sacoglossan sea slugs, such as C. tomentosum [ 64 ], and A. acetabulum [ 59 ]. Moreover, the most abundant PUFA in E. crispata was 20:4 n -6.…”

“…The amount of FA classes depends on gastropod species [ 31 ]. Some gastropod herbivores have higher amounts of PUFA, for instance, in Littorina littorea these FAs account for 52% of total lipids [ 32 ], and in E. timida represents 57% [ 59 ]. In this study, PUFA in E. crispata represents around 35% of the total pool of FAs, while in chromodorid nudibranchs, which feed on sponges, it accounts for 15–31% [ 65 ].…”

Ultraviolet screening by slug tissue and tight packing of plastids protect photosynthetic sea slugs from photoinhibition

“…It is generally accepted that in such times the slugs do benefit from the plastids, but whether this benefit is achieved by active transport of photosynthates or simply slow digestion of the plastids remains controversial (Christa et al 2014;Cartaxana et al 2017;Laetz et al 2017;Frankenbach et al 2021). It was recently suggested that metabolites produced in the plastids could be directed specifically for reproduction rather than adult slug household metabolism (Cruz et al 2020;Cartaxana et al 2021).…”

Crustaceans and Marine Heterobranchia: A New Symbiotic Relationship in the Mediterranean Sea

“…Elysia timida (Risso, 1818) is a "solar-powered" sacoglossan species (Mollusca, Gastropoda) long-studied for its ability to incorporate chloroplasts obtained from the algae it feeds on [1,2]. This species is endemic to the Mediterranean Sea and lives on rocky substrates at shallow water where it is locally common and often quite abundant (Figure 1).…”