Shedding light on starvation in darkness in the plastid-bearing sea slug Elysia viridis (Montagu, 1804)

Abstract

Sacoglossa are known for stealing photosynthetically active chloroplasts from their macroalgal food and incorporating them into their cytosol. The nutritional support these alien organelles (kleptoplasts) provide to the slugs is still debatable. Comparing slugs starved in continuous darkness (non-photosynthetic condition) and light (photosynthetic condition) is often used to understand the contribution of the kleptoplasts to the slugs' metabolism. Here, we examined the slugs' side of starvation in darkness to better understand the effects of darkness on the slugs. We compared the gene expression profile and digestive activity of Elysia viridis, starved for one week under ambient light and continuous darkness. Starvation in darkness led to the up-regulation of genes related to glucose deficiency, while genes involved in the development, cellular organization, and reproduction were down-regulated. This specific gene expression may counteract reduced nutrient availability under non-photosynthetic conditions. Under photosynthetic conditions, kleptoplasts may have a higher nutritional value and may be able to support some metabolic processes. It appears that the slugs can only access kleptoplast photosynthates through autophagy during starvation. Nevertheless, autophagy and length reduction in darkness are highly elevated compared to light conditions, suggesting that more slug tissue is needed to satisfy the nutritional demands under non-photosynthetic conditions. Since we did not detect a gene expression related to the export of photosynthates to the slugs, our results support the hypothesis that slugs use kleptoplasts as larders accessible via autophagy. As long as the kleptoplasts are functional, they provide an energetic support, helping the slugs to reduce starvation-induced stress.