Marine sacoglossa sea slugs, mainly of the family Plakobranchidea, have developed a unique functional nutritional mode in which they gain the capacity for phototrophic-mediated carbon acquisition using “stolen” chloroplasts. Rather than hosting algae endosymbionts, as found in nudibranchs, sacoglossa slugs graze on green siphonaceous macroalgae and sequester plastids into tubule cells of their digestive diverticula, a mechanism often named kleptoplasty.

Exposure to excessive light is expected to be a major cause of stress to the photosynthetic apparatus of photosynthetic symbioses. When the absorbed light energy exceeds the capacity of photochemical pathways, reactive oxidative species (ROS) accumulate in the cell and cause damages to the photosynthetic apparatus (photoinhibition), mainly through the degradation of protein D1 in photosystem (PS) II (Edelman and Mattoo 2008).  To cope with high ambient light levels, algae and plants have developed a range of physiological photoprotective processes, the most important being: (i) the xanthophyll cycle (XC), enabling the dissipation of excessive absorbed light energy as heat, (ii) the antioxidant enzyme system, scavenging for intracellular ROS, and (iii) the de novo synthesis of D1 protein, repairing photoinhibitory damages caused to PSII. In the case of marine photosynthetic symbioses typically inhabiting surface waters or intertidal habitats, the efficient functioning of photoprotective mechanisms may be of crucial importance for their survival as photoinhibition reduces the amount of photosynthetically fixed carbon made available to the animal host and damage the photosynthetic apparatus in the chloroplast. For instance, it is well known that the accumulation of ROS of photosynthetic origin in coral tissues is the cause of expulsion of zooxanthellae (“coral bleaching”) and the disruption of the symbiosis. In addition to physiological processes that can avoid photoinhibition, motile kleptoplasts-bearing animals have the possibility of using motility to avoid high light and such photobehaviour may be of photoprotective value. For instance, lateral body flaps (parapodia) that cover the dorsal surface of some sacoglossan slugs can play a role on the shielding of chloroplasts to excessive light, however, it is not known if this behaviour is common to all sacoglossan slugs in possession of parapodia. Anatomical and behavioural traits may together enhance the performance and functional longevity of chloroplasts in different light regimes, and hence optimize the energy budget of these slugs. This adaptation would be functionally equivalent to chloroplast avoidance movements and leaf fold described in plants and the migratory behaviour of motile microalgae, shown to provide effective photoprotection against photoinhibition.

In the case of plastid sequestration during sacoglossan development, it has been hypothesized that genes may have been transferred from algae to slugs, as several components of photosystems in active algal plastids display short lifespans (turnover times of the order of hours or less under bright light). Thus, if the photosynthetic machinery is turned over quickly, but plastids are maintained in an active state for weeks or even months, algal nuclear genes are suspected to be involved in plastid development, function, and maintenance in these sacoglossans. A horizontal gene transfer hypothesis [HGT] has been suggested after identification of algal nuclear genes in Elysia chlorotica. However, it was found that nuclear-encoded algal-derived genes specific to photosynthetic functions were not expressed in Plakobranchus ocellatus neither in Elysia timida. An alternative hypothesis to the HGT model suggest that long-term, functional kleptoplasty in E. chlorotica may result from a combination of yet-to-be characterized physical and molecular mechanisms; more specifically, unusual plastid stability combined with some degree of HGT, and long-term maintenance of cryptic algal products (DNA, RNA and proteins) that may persist for months after last chloroplasts ingestion. Additional sea slugs transcriptome and genome data are needed to assess these contrasting viewpoints on the maintenance of photosynthesis in sea slugs.

This work will provide new insights into the photophysiology and photobehaviour of Elysia viridis, a marine photosynthetic symbiose model occurring in North-eastern Atlantic temperate waters, and will advance the knowledge of how kleptoplasts are maintained photosynthetically active inside the animal, long after being ingested.

Research objectives

The main research objective of this project is to study the physiological and behavioural photoprotective processes preventing the occurrence of oxidative stress in Elysia viridis. This objective breaks down into four specific goals:

i) Characterize E. viridis behavioural responses to high light;

ii) Identify the main physiological processes involved in the photoprotection of kleptoplasts;

iii) Compare the relative efficiency of different photoprotective mechanisms in different prey (macroalgae);

iv) Clarify the degree of functional autonomy of kleptoplasts.

CESAM members on this project

João Serôdio

Ricardo Jorge Guerra Calado

Sónia Marisa Gonçalves da Cruz