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.