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

Abstract

Several sacoglossan sea slugs (Plakobranchoidea) feed upon plastids of large unicellular algae. Four species-called long-term retention (LtR) species-are known to sequester ingested plastids within specialized cells of the digestive gland. There, the stolen plastids (kleptoplasts) remain photosynthetically active for several months, during which time LtR species can survive without additional food uptake. Kleptoplast longevity has long been puzzling, because the slugs do not sequester algal nuclei that could support photosystem maintenance. It is widely assumed that the slugs survive starvation by means of kleptoplast photosynthesis, yet direct evidence to support that view is lacking. We show that two LtR plakobranchids, Elysia timida and Plakobranchus ocellatus, incorporate 14 CO 2 into acid-stable products 60-and 64-fold more rapidly in the light than in the dark, respectively. Despite this light-dependent CO 2 fixation ability, light is, surprisingly, not essential for the slugs to survive starvation. LtR animals survived several months of starvation (i) in complete darkness and (ii) in the light in the presence of the photosynthesis inhibitor monolinuron, all while not losing weight faster than the control animals. Contrary to current views, sacoglossan kleptoplasts seem to be slowly digested food reserves, not a source of solar power.

Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda)

“…Yet in our analyses, even NR forms and a non-sacoglossan slug, Phyllaplysia, are able to starve up for distinct periods. Thus, in these peculiar species, photosynthesis seems not to be essential for survival of starvation periods, as was also already hypothesized for three LtR forms (Christa et al 2014a, c).…”

“…The plastids of the algal food are then maintained by the slug, for which the term functional kleptoplasty was established (Rumpho et al 2006;Waugh and Clark 1986;Wägele and Martin 2013). How the slugs benefit from the kleptoplasts, e.g., via transfer of photosynthates from plastids into the cell lumen (Gallop 1974;Trench and Gooday 1973), is still unknown, and despite results of former studies (Giménez-Casalduero and Muniain 2008;Hinde and Smith 1975;Trench 1975), there is nowadays evidence that the slugs are not photoautotrophic (Christa et al 2014a, b).…”

Variable retention of kleptoplast membranes in cells of sacoglossan sea slugs: plastids with extended, shortened and non-retained durations

“…The denuded chloroplasts with stacks of thylakoid membranes and stroma with ribosomes appeared compact. They were shown to be able to photosynthesize (Händeler et al 2009;Christa et al 2014) and therefore must have endogenous functionally active systems operating in autonomous plastids (Green et al 2000).…”

Switching off photosynthesis

“…Costasiella ocellifera, Elysia viridis , E. chlorotica , E. timida and P. ocellatus have all been demonstrated to fix CO 2 in a light dependent manner 1 , 6 - 8 . But for how long during starvation, and is the amount of fixed CO 2 sufficient for them to really grow?…”