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Abstract
Some sacoglossan sea slugs incorporate intracellular functional algal chloroplasts, a process termed kleptoplasty. “Stolen” chloroplasts (kleptoplasts) can remain photosynthetically active up to several months, contributing to animal nutrition. Whether this contribution occurs by means of translocation of photosynthesis-derived metabolites from functional kleptoplasts to the animal host or by simple digestion of such organelles remains controversial. Imaging of 13C and 15N assimilation over a 12-h incubation period of Elysia viridis sea slugs showed a light-dependent incorporation of carbon and nitrogen, observed first in digestive tubules and followed by a rapid accumulation into chloroplast-free organs. Furthermore, this work revealed the presence of 13C-labeled long-chain fatty acids (FA) typical of marine invertebrates, such as arachidonic (20:4n-6) and adrenic (22:4n-6) acids. The time frame and level of 13C- and 15N-labeling in chloroplast-free organs indicate that photosynthesis-derived primary metabolites were made available to the host through functional kleptoplasts. The presence of specific 13C-labeled long-chain FA, absent from E. viridis algal food, indicates animal based-elongation using kleptoplast-derived FA precursors. Finally, carbon and nitrogen were incorporated in organs and tissues involved in reproductive functions (albumin gland and gonadal follicles), implying a putative role of kleptoplast photosynthesis in the reproductive fitness of the animal host.
Highlights
Kleptoplasty is the capacity of a non-photosynthetic host to retain functional chloroplasts from algal sources[1]
Isotopic dual labeling pulse experiments were conducted with E. viridis individuals incubated for 12 h with 13C-bicarbonate and 15N-ammonium
The fatty acids (FA) 22:5n-3, which was abundant in E. viridis, can be produced from its precursor 20:5n-333, the latter being present in C. tomentosum[32] but displaying a much higher relative abundance in E. viridis
Summary
Kleptoplasty is the capacity of a non-photosynthetic host to retain functional chloroplasts from algal sources ( termed kleptoplasts or kleptochloroplasts)[1]. The detection of radioactivity in kleptoplast-free organs at such sort-time frame was indicative of incorporation via functional kleptoplasts in these two species In another species, Elysia timida, it was recently proposed that, after some days of starvation, starch accumulated at the kleptoplasts and could be used by the animal after kleptoplast digestion[18,19]. Elysia timida, it was recently proposed that, after some days of starvation, starch accumulated at the kleptoplasts and could be used by the animal after kleptoplast digestion[18,19] Another potential benefit mediated by kleptoplasty that remains unexplored in photosynthetic sea slugs is nitrogen assimilation. This work presents new evidence for light-dependent incorporation of inorganic carbon and nitrogen into tissues of the sacoglossan sea slug Elysia viridis, using compound specific isotope analysis (CSIA) of fatty acid methyl esters (FAME) coupled with high-resolution secondary ion mass spectrometry (NanoSIMS), demonstrating spatial and temporal movements of 13C and 15N isotopes
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