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

Authors
  • Cruz, Sónia1
  • LeKieffre, Charlotte1, 2, 3
  • Cartaxana, Paulo1
  • Hubas, Cédric4
  • Thiney, Najet4
  • Jakobsen, Sofie5
  • Escrig, Stéphane6
  • Jesus, Bruno7
  • Kühl, Michael5
  • Calado, Ricardo1
  • Meibom, Anders6, 8
  • 1 ECOMARE, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, Aveiro, 3810-193, Portugal , Aveiro (Portugal)
  • 2 UMR CNRS 6112 LPG-BIAF, Université d’Angers, 2 Boulevard Lavoisier, Angers, Cedex 1, 49045, France , Angers (France)
  • 3 Cell & Plant Physiology Laboratory, University of Grenoble Alpes, CNRS, CEA, INRA, Grenoble, France , Grenoble (France)
  • 4 Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Muséum National d’Histoire Naturelle, Sorbonne Université, Université de Caen Normandie, Université des Antilles, CNRS, IRD, Station Marine de Concarneau, Place de la croix, Concarneau, 29900, France , Concarneau (France)
  • 5 Marine Biological Section, Department of Biology, University of Copenhagen, Helsingør, 3000, Denmark , Helsingør (Denmark)
  • 6 Laboratory for Biological Geochemistry, École Polytechnique Fédérale de Lausanne, Lausanne, 1015, Switzerland , Lausanne (Switzerland)
  • 7 Laboratoire Mer Molécules Santé, Faculté des Sciences et des Techniques, Université de Nantes, Nantes, 44322, France , Nantes (France)
  • 8 Center for Advanced Surface Analysis, Institute of Earth Sciences, University of Lausanne, Lausanne, 1015, Switzerland , Lausanne (Switzerland)
Type
Published Article
Journal
Scientific Reports
Publisher
Springer Nature
Publication Date
Jun 29, 2020
Volume
10
Issue
1
Identifiers
DOI: 10.1038/s41598-020-66909-7
Source
Springer Nature
License
Green

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.

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