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 13C and 15N 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.
Highlights
Sacoglossa is a group of sap-sucking sea slugs that feed on macroalgae
We investigated the putative role of kleptoplast photosynthesis in the reproduction of the sacoglossan sea slug Elysia timida by (i) tracking short-term light-dependent incorporation of inorganic carbon and nitrogen into animal tissues using compound-specific isotope analysis (CSIA) of fatty acid methyl esters (FAMEs) and high-resolution secondary ion mass spectrometry (NanoSIMS), and (ii) investigating the effects of limiting photosynthesis in the number and fatty acid (FA) composition of spawned eggs
Light-dependent carbon incorporation was not restricted to these kleptoplastbearing cells, and rapid accumulation was observed in kleptoplast-free organs such as the albumen gland and gonadal follicles.13C incorporation was not detected in the tissues of E. timida exposed to full darkness
Summary
The most striking feature of some of these sea slugs is their ability to digest the algal cellular content while retaining intact functional chloroplasts (kleptoplasts) within the cells of their digestive gland [1,2]. We investigated the putative role of kleptoplast photosynthesis in the reproduction of the sacoglossan sea slug Elysia timida by (i) tracking short-term light-dependent incorporation of inorganic carbon and nitrogen into animal tissues using compound-specific isotope analysis (CSIA) of fatty acid methyl esters (FAMEs) and high-resolution secondary ion mass spectrometry (NanoSIMS), and (ii) investigating the effects of limiting photosynthesis (rearing animals under reduced light levels) in the number and fatty acid (FA) composition of spawned eggs. We report strong experimental evidence for a role of photosynthesis in the reproductive investment and fitness of a kleptoplast-bearing sea slug
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