Kleptoplast photosynthesis is nutritionally relevant in the sea slug Elysia viridis

Paulo Cartaxana,Sónia Cruz,Erik Trampe,Michael Kühl

doi:10.1038/s41598-017-08002-0

Paulo Cartaxana, Sónia Cruz + Show 2 more

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https://doi.org/10.1038/s41598-017-08002-0

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Abstract

Several sacoglossan sea slug species feed on macroalgae and incorporate chloroplasts into tubular cells of their digestive diverticula. We investigated the role of the “stolen” chloroplasts (kleptoplasts) in the nutrition of the sea slug Elysia viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation. Elysia viridis individuals feeding on the macroalga Codium tomentosum were compared with starved specimens kept in dark and low light conditions. A combination of variable Chl a fluorescence and hyperspectral imaging, and HPLC pigment analysis was used to evaluate the spatial and temporal variability of photopigments and of the photosynthetic capacity of kleptoplasts. We show increased loss of weight and body length in dark-starved E. viridis as compared to low light-starved sea slugs. A more pronounced decrease in kleptoplast abundance and lower photosynthetic electron transport rates were observed in dark-starved sea slugs than in low light-starved animals. This study presents strong evidence of the importance of kleptoplast photosynthesis for the nutrition of E. viridis in periods of food scarcity. Deprived of photosynthates, E. viridis could accelerate the breakdown of kleptoplasts in the dark to satisfy its’ energy requirements.

Highlights

Mixotrophic organisms are able to obtain organic carbon via both heterotrophic and phototrophic metabolisms[1], and include several sacoglossan sea slug species that use their radular teeth to penetrate the cell wall of algal filaments, suck and digest the cellular content, while incorporating functional algal chloroplasts into tubular cells of their digestive diverticula via a process known as kleptoplasty[2, 3]
We investigated the role of kleptoplasts in the nutrition of the sacoglossan sea slug E. viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation
Hinde & Smith[17] found a more pronounced decrease in weight of E. viridis kept in the dark and argued that observed rates of photosynthesis were sufficient to account for the observed weight differences

Summary

Introduction

Mixotrophic organisms are able to obtain organic carbon via both heterotrophic and phototrophic metabolisms[1], and include several sacoglossan sea slug species that use their radular teeth to penetrate the cell wall of algal filaments, suck and digest the cellular content, while incorporating functional algal chloroplasts into tubular cells of their digestive diverticula via a process known as kleptoplasty[2, 3] These acquired chloroplasts – commonly termed kleptoplasts – do not divide[4], but may remain functional for periods ranging from a few days to several months[5, 6]. New imaging techniques such as Chl a fluorescence and hyperspectral imaging have been used to map pigment content and photosynthetic activity in microbial phototrophs and symbioses[13,14,15] as well as kleptoplastidic dinoflagellates[16] Such techniques allow the assessment of spatial differences on scales ranging from the single-cell to areas of several square centimeters, improving our capacity to understand spatial and functional relationships. We addressed the following questions: i) Does blocking of photosynthesis through light deprivation in the absence of their algal food source increase the loss of sea slug body weight and length? ii) Are kleptoplasts of E. viridis kept in the dark as photosynthetically competent as kleptoplasts maintained under light/dark cycles? iii) How is kleptoplast abundance and distribution in E. viridis affected by starvation and light/dark conditions?

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