Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs

Elysia chlorotica is a kleptoplastic sea slug that preys on Vaucheria litorea, stealing its plastids which then continue to photosynthesize for months inside the animal cells. We investigated the native properties of V. litorea plastids to understand how they withstand the rigors of photosynthesis in isolation. Transcription of specific genes in laboratory-isolated V. litorea plastids was monitored up to seven days. The involvement of plastid-encoded FtsH, a key plastid maintenance protease, in recovery from photoinhibition in V. litorea was estimated in cycloheximide-treated cells. In vitro comparison of V. litorea and spinach thylakoids was applied to investigate ROS formation in V. litorea. Isolating V. litorea plastids triggered upregulation of ftsH and translation elongation factor EF-Tu (tufA). Upregulation of FtsH was also evident in cycloheximide-treated cells during recovery from photoinhibition. Charge recombination in PSII of V. litorea was found to be fine-tuned to produce only small quantities of singlet oxygen (1O2). Our results support the view that the genetic characteristics of the plastids themselves are crucial in creating a photosynthetic sea slug. The plastid’s autonomous repair machinery is likely enhanced by low 1O2 production and by upregulation of FtsH in the plastids.HighlightIsolated Vaucheria litorea plastids exhibit upregulation of tufA and ftsH, key plastid maintenance genes, and produce only little singlet oxygen. These factors likely contribute to plastid longevity in kleptoplastic slugs.

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

The sea slug Elysia chlorotica acquires plastids by ingestion of its algal food source Vaucheria litorea. Organelles are sequestered in the mollusc's digestive epithelium, where they photosynthesize for months in the absence of algal nucleocytoplasm. This is perplexing because plastid metabolism depends on the nuclear genome for >90% of the needed proteins. Two possible explanations for the persistence of photosynthesis in the sea slug are (i) the ability of V. litorea plastids to retain genetic autonomy and/or (ii) more likely, the mollusc provides the essential plastid proteins. Under the latter scenario, genes supporting photosynthesis have been acquired by the animal via horizontal gene transfer and the encoded proteins are retargeted to the plastid. We sequenced the plastid genome and confirmed that it lacks the full complement of genes required for photosynthesis. In support of the second scenario, we demonstrated that a nuclear gene of oxygenic photosynthesis, psbO, is expressed in the sea slug and has integrated into the germline. The source of psbO in the sea slug is V. litorea because this sequence is identical from the predator and prey genomes. Evidence that the transferred gene has integrated into sea slug nuclear DNA comes from the finding of a highly diverged psbO 3′ flanking sequence in the algal and mollusc nuclear homologues and gene absence from the mitochondrial genome of E. chlorotica. We demonstrate that foreign organelle retention generates metabolic novelty (“green animals”) and is explained by anastomosis of distinct branches of the tree of life driven by predation and horizontal gene transfer.