Transcriptomic Evidence That Longevity of Acquired Plastids in the Photosynthetic Slugs Elysia timida and Plakobranchus ocellatus Does Not Entail Lateral Transfer of Algal Nuclear Genes

Abstract

Sacoglossan sea slugs are unique in the animal kingdom in that they sequester and maintain active plastids that they acquire from the siphonaceous algae upon which they feed, making the animals photosynthetic. Although most sacoglossan species digest their freshly ingested plastids within hours, four species from the family Plakobranchidae retain their stolen plastids (kleptoplasts) in a photosynthetically active state on timescales of weeks to months. The molecular basis of plastid maintenance within the cytosol of digestive gland cells in these photosynthetic metazoans is yet unknown but is widely thought to involve gene transfer from the algal food source to the slugs based upon previous investigations of single genes. Indeed, normal plastid development requires hundreds of nuclear-encoded proteins, with protein turnover in photosystem II in particular known to be rapid under various conditions. Moreover, only algal plastids, not the algal nuclei, are sequestered by the animals during feeding. If algal nuclear genes are transferred to the animal either during feeding or in the germ line, and if they are expressed, then they should be readily detectable with deep-sequencing methods. We have sequenced expressed mRNAs from actively photosynthesizing, starved individuals of two photosynthetic sea slug species, Plakobranchus ocellatus Van Hasselt, 1824 and Elysia timida Risso, 1818. We find that nuclear-encoded, algal-derived genes specific to photosynthetic function are expressed neither in P. ocellatus nor in E. timida. Despite their dramatic plastid longevity, these photosynthetic sacoglossan slugs do not express genes acquired from algal nuclei in order to maintain plastid function.

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

“…Clearly, there is no algal genomic support (Pelletreau et al, 2011;Wägele et al, 2011;Bhattacharya et al, 2013), neither through remnants of an algae nucleus nor through a eukaryotic horizontal gene transfer (Rauch et al, 2015). It is still unknown whether the slugs are able to actively support the kleptoplasts to stay functional.…”

“…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).…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…A partial transcriptome analysis of two other sea slug species, Elysia timida and Plakobranchus ocellatus has revealed no evidence of transcripts corresponding to algal genes [44]. Another report has also failed to detect evidence of the transcription of presumptive transferred genes in E. chlorotica [45].…”

Plastid-bearing sea slugs fix CO2in the light but do not require photosynthesis to survive

“…Because these four species can maintain plastids with functional photosystems for several months, they are designated as long-term retention (LtR) species in contrast to those plakobranchids that are only able to maintain functional plastids for up to two weeks, and which are hence termed short-term retention (StR) species [7]. In E. timida, the undigested plastids remain ultrastructurally intact and photosynthetically active, as determined by photosystem fluorescence, for more than two months [7,8]. Having acquired a load of plastids, the animals can be kept in the laboratory, in the light, for months without additional food [7][8][9][10].…”

“…In E. timida, the undigested plastids remain ultrastructurally intact and photosynthetically active, as determined by photosystem fluorescence, for more than two months [7,8]. Having acquired a load of plastids, the animals can be kept in the laboratory, in the light, for months without additional food [7][8][9][10].…”