TY - JOUR

T1 - Functional kleptoplasts intermediate incorporation of carbon and nitrogen in cells of the Sacoglossa sea slug Elysia viridis

AU - Cruz, Sónia

AU - LeKieffre, Charlotte

AU - Cartaxana, Paulo

AU - Hubas, Cédric

AU - Thiney, Najet

AU - Jakobsen, Sofie

AU - Escrig, Stéphane

AU - Jesus, Bruno

AU - Kühl, Michael

AU - Calado, Ricardo

AU - Meibom, Anders

PY - 2020

Y1 - 2020

N2 - 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.

AB - 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.

KW - FATTY-ACIDS

KW - CODIUM-FRAGILE

KW - CHLOROPLASTS

KW - OPISTHOBRANCHIA

KW - ASSOCIATION

KW - GASTROPODA

KW - PHOTOSYNTHESIS

KW - BIOSYNTHESIS

KW - METABOLISM

KW - ORGANELLES

U2 - 10.1038/s41598-020-66909-7

DO - 10.1038/s41598-020-66909-7

M3 - Journal article

C2 - 32601288

VL - 10

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

M1 - 10548

ER -