Comparison of sister species identifies factors underpinning plastid compatibility in green sea slugs

Abstract

The only animal cells known that can maintain functional plastids (kleptoplasts) in their cytosol occur in the digestive gland epithelia of sacoglossan slugs. Only a few species of the many hundred known can profit from kleptoplasty during starvation long-term, but why is not understood. The two sister taxa Elysia cornigera and Elysia timida sequester plastids from the same algal species, but with a very different outcome: while E. cornigera usually dies within the first two weeks when deprived of food, E. timida can survive for many months to come. Here we compare the responses of the two slugs to starvation, blocked photosynthesis and light stress. The two species respond differently, but in both starvation is the main denominator that alters global gene expression profiles. The kleptoplasts' ability to fix CO2 decreases at a similar rate in both slugs during starvation, but only E. cornigera individuals die in the presence of functional kleptoplasts, concomitant with the accumulation of reactive oxygen species (ROS) in the digestive tract. We show that profiting from the acquisition of robust plastids, and key to E. timida's longer survival, is determined by an increased starvation tolerance that keeps ROS levels at bay.

Life Cycle Analysis of Endosymbiotic Algae in an Endosymbiotic Situation with Paramecium bursaria Using Capillary Flow Cytometry

“…Several ongoing plastid-acquisition types of endosymbiosis are observed in sacoglossan sea slugs such as Elysia chlorotica and E. timida [11,[35][36][37], and in the marine ciliate Mesodinium rubrum [38][39][40][41]. However, they are defective in their ability to maintain permanent endosymbiosis.…”

Photoprotective Non-photochemical Quenching Does Not Prevent Kleptoplasts From Net Photoinactivation

“…About 2,000 proteins are needed to support photosynthesis in algae and plants, but only a fraction is encoded in the genome of plastids (Timmis et al, 2004) and none of the relevant genes were found in the slugs' genomes investigated so far (Wägele et al, 2011;Bhattacharya et al, 2013;de Vries et al, 2015;Han et al, 2015). This led to the search for alternative factors that enable kleptoplast longevity, and plastid photoprotection mechanisms came into focus (Jesus et al, 2010;Cruz et al, 2015).…”

Animal biosynthesis of complex polyketides in a photosynthetic partnership

“…Sacoglossan transcriptome reads were acquired in previous work by other groups 11,23 from 19 specimens of Elysia chlorotica, Elysia timida , and Elysia cornigera (Extended Data Table 3). We downloaded the reads from the NCBI Sequence Read Archive (SRA) and assembled them using IDBA-UD 44 .…”

“…We were unable to identify good candidate polypropionate synthases from the bacterial metagenomes, suggesting a possible origin in the animals or chloroplasts. We took advantage of recently released genomes and transcriptomes of three sacoglossans 11,22–24 , Elysia chlorotica, E. timida , and E. cornigera , to test this hypothesis. E. chlorotica contains polypropionates ent -9,10-deoxytridachione and elysione 25 , while E. timida contains ent -9,10-deoxytridachione and several relatives (Fig.…”