Mucopolysaccharides secreted by the sea slug Elysia crispata incorporate carbon via kleptoplast photosynthesis

abstract

Some Sacoglossa sea slugs feed on macroalgae and sequester chloroplasts in the cells of their digestive diverticulum. In some species, mostly within the genus Elysia, the stolen chloroplasts - kleptoplasts - remain photosynthetically competent for weeks to months. These sea slugs, like other gastropods, produce a viscous secretion or mucus involved in protection, locomotion, and reproduction. In this study, we profiled the carbohydrate composition of the mucus of the kleptoplast-bearing sea slug Elysia crispata and tracked the incorporation of carbon and nitrogen via stolen chloroplasts. Mucopolysaccharides were mainly composed by uronic acids and galactose with 1 -> 4 glycosidic linkages. Using inorganic 13C-labelled sea water, incorporated carbon was found in the secreted mucus only in the presence of light, mainly in the form of 3-O-methylgalactose, galactose, and fucose. Inorganic 15N in the sea water could be traced in the sea slug tissues and in the mucus in both dark and light, with slightly higher levels found under the latter condition. Results show that inorganic carbon was fixed through photosynthesis in the kleptoplasts of the digestive diverticula, translocated as organic carbon to other animal tissues and incorporated in the secreted mucopolysaccharides. The present study pinpoints the biological relevance of photosynthesis to the metabolism of these remarkable animal-chloroplast symbiotic associations.

keywords

ANION-EXCHANGE CHROMATOGRAPHY; CELL-WALL POLYSACCHARIDES; CARBOHYDRATE-COMPOSITION; FUNCTIONAL CHLOROPLASTS; SYMBIOTIC CHLOROPLASTS; MUCUS SYNTHESIS; CODIUM-FRAGILE; OPISTHOBRANCHIA; ASSOCIATION; RETENTION

subject category

Environmental Sciences & Ecology; Marine & Freshwater Biology

authors

Lopes, D; Cartaxana, P; Ferreira, SS; Silva, MI; Nunes, M; Barata, J; Nunes, C; Cruz, S

Groups

G4 - Renewable Materials and Circular Economy

Projects

CICECO - Aveiro Institute of Materials (UIDB/50011/2020)

CICECO - Aveiro Institute of Materials (UIDP/50011/2020)

Associated Laboratory CICECO-Aveiro Institute of Materials (LA/P/0006/2020)

acknowledgements

The author(s) declare that financial support was received for the research and/or publication of this article. This work was supported by the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme, grant agreement no. 949880 to SC (DOI:10.3030/949880), and by Fundac & atilde;o para a Ciencia e Tecnologia, grants 2020.08672 BD to DL, 2020.03278.CEECIND to SC (DOI:10.54499/2020.03278.CEECIND/CP1589/CT0012), CEECIND/01434/2018 to PC (DOI:10.54499/CEECIND/01434/2018/CP1559/CT0003), UID + LA/P/0094/2020 to CESAM, UIDB/50006/2020 (DOI:10.54499/UIDB/50006/2020), UIDP/50006/2020 (DOI:10.54499/UIDP/50006/2020), and LA/P/0008/2020 (DOI:10.54499/LA/P/0008/2020) to LAQV/REQUIMTE, and UIDB/50011/2020 (DOI 10.54499/UIDB/50011/2020), UIDP/50011/2020 (DOI 10.54499/UIDP/50011/2020) and LA/P/0006/2020 (DOI 10.54499/LA/P/0006/2020) to CICECO.