Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis

Sónia Cruz*, Charlotte LeKieffre, Paulo Cartaxana, Cédric Hubas, Najet Thiney, Sofie Jakobsen, Stéphane Escrig, Bruno Jesus, Michael Kühl, Ricardo Calado, Anders Meibom

*Corresponding author for this work

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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 C-13 and N-15 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 C-13-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 C-13- and N-15-labeling in chloroplast-free organs indicate that photosynthesis-derived primary metabolites were made available to the host through functional kleptoplasts. The presence of specific C-13-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.

Original languageEnglish
Article number10548
JournalScientific Reports
Volume10
Number of pages12
ISSN2045-2322
DOIs
Publication statusPublished - 2020

Keywords

  • FATTY-ACIDS
  • CODIUM-FRAGILE
  • CHLOROPLASTS
  • OPISTHOBRANCHIA
  • ASSOCIATION
  • GASTROPODA
  • PHOTOSYNTHESIS
  • BIOSYNTHESIS
  • METABOLISM
  • ORGANELLES

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