Photosynthesis from stolen chloroplasts can support sea slug reproductive fitness

Author:

Cartaxana Paulo12ORCID,Rey Felisa13,LeKieffre Charlotte4ORCID,Lopes Diana1,Hubas Cédric5ORCID,Spangenberg Jorge E.6ORCID,Escrig Stéphane7,Jesus Bruno8ORCID,Calado Gonçalo910,Domingues Rosário23,Kühl Michael11ORCID,Calado Ricardo1ORCID,Meibom Anders712ORCID,Cruz Sónia1ORCID

Affiliation:

1. CESAM—Centre for Environmental and Marine Studies, University of Aveiro, Aveiro 3810-193, Portugal

2. Department of Biology, University of Aveiro, Aveiro 3810-193, Portugal

3. Mass Spectrometry Centre, LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, Aveiro 3810-193, Portugal

4. Cell and Plant Physiology Laboratory, University of Grenoble Alpes, CNRS, CEA, INRAE, Grenoble Cedex, France

5. Biologie des Organismes et Écosystèmes Aquatiques (UMR BOREA 8067), 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

6. Institute of Earth Surface Dynamics (IDYST), University of Lausanne, Lausanne, CH-1015, Switzerland

7. Laboratory for Biological Geochemistry, École Polytechnique Fédérale de Lausanne, Lausanne, CH-1015, Switzerland

8. Laboratoire Mer Molécules Santé, Faculté des Sciences et des Techniques, Université de Nantes, Nantes 44322, France

9. Department of Life Sciences, Lusófona University, Campo Grande 376, Lisbon 1749-024, Portugal

10. NOVA School of Science and Technology, MARE—Marine and Environmental Sciences Centre, Campus de Caparica, Caparica 2829-516, Portugal

11. Marine Biological Section, Department of Biology, University of Copenhagen, Strandpromenaden 5, Helsingør 3000, Denmark

12. Center for Advanced Surface Analysis, Institute of Earth Sciences, University of Lausanne, Lausanne, CH-1015, Switzerland

Abstract

Some sea slugs are able to steal functional chloroplasts (kleptoplasts) from their algal food sources, but the role and relevance of photosynthesis to the animal host remain controversial. While some researchers claim that kleptoplasts are slowly digestible ‘snacks’, others advocate that they enhance the overall fitness of sea slugs much more profoundly. Our analysis shows light-dependent incorporation of 13 C and 15 N in the albumen gland and gonadal follicles of the sea slug Elysia timida , representing translocation of photosynthates to kleptoplast-free reproductive organs. Long-chain polyunsaturated fatty acids with reported roles in reproduction were produced in the sea slug cells using labelled precursors translocated from the kleptoplasts. Finally, we report reduced fecundity of E. timida by limiting kleptoplast photosynthesis. The present study indicates that photosynthesis enhances the reproductive fitness of kleptoplast-bearing sea slugs, confirming the biological relevance of this remarkable association between a metazoan and an algal-derived organelle.

Funder

H2020 European Research Council

Fundação para a Ciência e a Tecnologia

Gordon and Betty Moore Foundation

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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