Photosynthetic sea slugs induce protective changes to the light reactions of the chloroplasts they steal from algae

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Abstract

Sacoglossan sea slugs are able to maintain functional chloroplasts inside their own cells, and mechanisms that allow preservation of the chloroplasts are unknown. We found that the slug Elysia timida induces changes to the photosynthetic light reactions of the chloroplasts it steals from the alga Acetabularia acetabulum. Working with a large continuous laboratory culture of both the slugs (>500 individuals) and their prey algae, we show that the plastoquinone pool of slug chloroplasts remains oxidized, which can suppress reactive oxygen species formation. Slug chloroplasts also rapidly build up a strong proton motive force upon a dark-to-light transition, which helps them to rapidly switch on photoprotective non-photochemical quenching of excitation energy. Finally, our results suggest that chloroplasts inside E. timida rely on oxygen-dependent electron sinks during rapid changes in light intensity. These photoprotective mechanisms are expected to contribute to the long-term functionality of the chloroplasts inside the slugs.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2, 3, 4, Figure 4-figure supplement 1 and Figures 5, 6, 7B-E and 8.

Article and author information

Author details

Vesa Havurinne

Biochemistry, University of Turku, Turku, Finland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5213-0905
Esa Tyystjärvi

Biochemistry, University of Turku, Turku, Finland

For correspondence
esatyy@utu.fi

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6808-7470

Funding

Academy of Finland (307335)

Esa Tyystjärvi

Suomen Kulttuurirahasto (Graduate student grant)

Vesa Havurinne

Suomalainen Tiedeakatemia (Graduate student grant)

Vesa Havurinne

University of Turku graduate school, DPMLS (Graduate student grant)

Vesa Havurinne

Academy of Finland (333421)

Esa Tyystjärvi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in accordance with EU legislation and directives concerning scientific research on non-cephalopod invertebrates.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.