Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis.
Cruz SECOMARE, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal. sonia.cruz@ua.pt.
LeKieffre CECOMARE, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal.
Cartaxana PECOMARE, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal.
Hubas CBiologie 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, 29900, Concarneau, France.
Thiney NBiologie 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, 29900, Concarneau, France.
Jakobsen SMarine Biological Section, Department of Biology, University of Copenhagen, 3000, Helsingør, Denmark.
Escrig SLaboratory for Biological Geochemistry, École Polytechnique Fédérale de Lausanne, 1015, Lausanne, Switzerland.
Jesus BLaboratoire Mer Molécules Santé, Faculté des Sciences et des Techniques, Université de Nantes, 44322, Nantes, France.
Kühl MMarine Biological Section, Department of Biology, University of Copenhagen, 3000, Helsingør, Denmark.
Calado RECOMARE, CESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal.
Meibom ALaboratory for Biological Geochemistry, École Polytechnique Fédérale de Lausanne, 1015, Lausanne, Switzerland.
English
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.