1. Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis
- Author
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Cédric Hubas, Michael Kühl, Stéphane Escrig, Sónia Cruz, Sofie L. Jakobsen, Bruno Jesus, Najet Thiney, Anders Meibom, Paulo Cartaxana, Ricardo Calado, Charlotte LeKieffre, Centre for Environmental and Marine Studies [Aveiro] (CESAM), Universidade de Aveiro, Laboratoire de Planétologie et Géodynamique - Angers (LPG-ANGERS), Laboratoire de Planétologie et Géodynamique [UMR 6112] (LPG), Université d'Angers (UA)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS), Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), Station de Biologie Marine de Concarneau, Direction générale déléguée à la Recherche, à l’Expertise, à la Valorisation et à l’Enseignement-Formation (DGD.REVE), Muséum national d'Histoire naturelle (MNHN)-Muséum national d'Histoire naturelle (MNHN), University of Copenhagen = Københavns Universitet (KU), Ecole Polytechnique Fédérale de Lausanne (EPFL), Mer, molécules et santé EA 2160 (MMS), Le Mans Université (UM)-Université de Nantes - UFR des Sciences et des Techniques (UN UFR ST), Université de Nantes (UN)-Université de Nantes (UN)-Université de Nantes - UFR des Sciences Pharmaceutiques et Biologiques, Université de Nantes (UN)-Université de Nantes (UN), FEDER, through COMPETE2020 - Programa Operacional Competitividade e InternacionalizacAo (POCI), Programa Operacional Regional (POR) de Lisboa national funds (OE), through FCT/MCTES PTDC/BIA-ANM/4622/2014POCI-01-0145-FEDER-016754CESAM through national funds (OE) via FCT/MCTES UIDB/50017/2020+UIDP/50017/2020Sapere-Aude advanced grant from the Independent Research Fund Denmark DFF-8021-00308BFCT/MCTES through Programa Investigador IF/00899/2014Portuguese Foundation for Science and TechnologyEuropean Commission, Muséum national d'Histoire naturelle (MNHN), University of Copenhagen = Københavns Universitet (UCPH), Institut Des Substances et Organismes de la Mer - UR 2160 (ISOMER), Nantes Université - UFR des Sciences Pharmaceutiques et Biologiques (Nantes Univ - UFR Pharmacie), Nantes Université - pôle Santé, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Santé, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes université - UFR des Sciences et des Techniques (Nantes univ - UFR ST), Nantes Université - pôle Sciences et technologie, Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Nantes Université - pôle Sciences et technologie, and Nantes Université (Nantes Univ)
- Subjects
0106 biological sciences ,0301 basic medicine ,CODIUM-FRAGILE ,Physiology ,lcsh:Medicine ,01 natural sciences ,CHLOROPLASTS ,lcsh:Science ,[SDV.EE]Life Sciences [q-bio]/Ecology, environment ,Multidisciplinary ,Ecology ,opisthobranchia ,[SDV.BA]Life Sciences [q-bio]/Animal biology ,Fatty Acids ,ASSOCIATION ,Chloroplast ,Biochemistry ,chloroplasts ,FATTY-ACIDS ,Kleptoplasty ,Elysia viridis ,Nitrogen ,[SDV.BC]Life Sciences [q-bio]/Cellular Biology ,METABOLISM ,Biology ,Photosynthesis ,010603 evolutionary biology ,GASTROPODA ,Article ,03 medical and health sciences ,Animals ,codium-fragile ,[CHIM]Chemical Sciences ,[SDV.BV]Life Sciences [q-bio]/Vegetal Biology ,BIOSYNTHESIS ,OPISTHOBRANCHIA ,photosynthesis ,Sacoglossa ,PHOTOSYNTHESIS ,lcsh:R ,association ,ORGANELLES ,Assimilation (biology) ,Marine invertebrates ,fatty-acids ,biology.organism_classification ,Carbon ,Sea slug ,030104 developmental biology ,organelles ,gastropoda ,lcsh:Q ,biosynthesis ,Plant sciences ,Zoology ,metabolism - 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.
- Published
- 2020