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I first heard about this species back in 2019. At the time, I was a biology student who was fascinated with the world. I was fascinated by how nature always finds a way to survive and differentiate, how life seems to be possible everywhere, but maybe not by our definitions.

Picture by Patrick J. Krug

Elysia chlorotica is a slug species capable of kleptoplasty, which is the retention and uptake of plastids due to feeding from algal prey. This is amazing, but it is even more fascinating because E.chlorotica does this only with the genus Vaucheria. This genus of algae does not have walls between adjoining cells, so the slug makes a hole in the outer cell wall and sucks out all the algal plastids at once. These plastids depend a lot on the nuclear genome from the algae to work; the nucleus supplies >90% of the proteins, but Elysia only ingests the chloroplasts. These slugs also do not complete metamorphosis and development without this alga and its chloroplasts. The plastids are solely responsible for animal development after just one week. If the supply of food is interrupted during the first week of development, the plastids break down, and E.chlorotica ceases to develop.

How does E.chlorotica recognise chloroplasts?

E.chlorotica is similar (genetically) to the other two species of sea slugs, E.cornigera and E.timida. These two species also feed on algae and sequester their chloroplasts, but they feed on different species of alga, Acetabularia acetabulum. The origin of the chloroplasts of A.acetabulum and V.litorea is quite different; A.acetabulum evolved from primary symbiosis in the chlorophyte lineage, while V. litorea evolved from a secondary endosymbiosis in the rhodophyte lineage. This difference leads to a different composition of lipopolysaccharides and glycans and other macromolecules on the chloroplasts’ membranes which might be related to their recognition by the host. Also, when the chloroplasts are ingested, interactions between the chloroplasts and the slug’s immune system take place to discriminate between plastids and possible pathogens that are harmful to the host. These are pattern recognition receptors (PRRs) of the host and microbe-associated molecular patterns (MAMPs) of the symbiont that trigger different signalling cascades that trigger the appropriate response.

How does Elysia chlorotica keep the plastids?

At first, it was proposed that Horizontal Gene Transfer between the algae and the slug’s germ line took place, but this has been disproved. Researchers at Rutgers University took DNA from E.chlorotica eggs that were never in contact with the algae and found that there was no presence of algal genes in the germ line of the sea slugs. Meaning that any genes from algae that were present in the slug were probably obtained after the plastids were ingested. 

Rumpho et al. ‘s team sequenced the plastid’s genome and confirmed that the chloroplasts lack the genetic apparatus required for photosynthesis. This team also found that the gene psbO, a nuclear gene of oxygenic photosynthesis, is expressed in the sea slug and is present in the germ line. Plastid’s DNA (ptDNA) lacked the main core protein, MSP (manganese stabilizing protein) (encoded by psbO) part of the photosystem II which is extremely important for photosynthesis. When water molecules split during photosynthesis, MSP stabilises the reaction that generates oxygen. However, this protein was never found in animal genomes, and neither did psbO, meaning that the slug had to get this protein by horizontal gene transfer (HGT). 

PsbO subunit of Photosystem II, beta barrel domain from cyanobacterium Thermosynechococcus vestitus (PDB ID: 5G3A).

The plastids supply energy and carbon for approximately 10 months, which allows E.chlorotica not to have to seek food. How does Elysia chlorotica prevent its system from expelling the chloroplasts? When a human gets an organ transplant, they have to take antirejection medication. Also, photosynthesis produces free oxygen radicals at levels that animals cannot tolerate. Plants have P700 (Photosystem I), which suppresses the production of these reactive oxygen species, but animals do not have this complex. How does E.chlorotica go around this? The plastids from V. litorea contain some genes that help with the longevity and functionality of the symbiosis. When E. chlorotica ingests the chloroplasts, PSII (photosystem II, protein required for photosynthesis) has charge recombination, which makes the plastid only produce small quantities of singlet oxygen, leading to low oxygen production but also decreases the number of free oxygen radicals. On top of that, the expression of translation elongation factor EF-Tu and FtsH protease increases during symbiosis. This protease is very critical for the repair of photosystem II from damage.

E.Chlorotica eating Vaucheria seaweed. Video from Rumpho et al. articles.

Immunosuppression

Chan et al. found that when the slug takes the chloroplasts, the sea slug’s immune system is suppressed by a group of proteins synthesised by the slug, to avoid rejection from its system. The team used RNA-Seq analysis to see if there were any traces of algae genes after ingestion of the plastids. After the experiment, the slugs showed an increase in the transcription of genes related to proteins associated with oxidative stress responses. The level of these biochemical reactions changes during symbiosis. When the slug is first exposed to the algae there is an increase in the MAMP-PPR signalling cascade, which is related to the recognition of a body as foreign. DNA repair genes also increase concentration. These responses show that the animal is in temporary distress. All this reverts as the symbiosis matures and ribosomes and phagosomes are permanently suppressed. This might suggest that the genes from the plastids complement E.chlorotica genes and how these interact in the long term.

Elysia chlorotica feeding on Vaucheria litorea.

E. chlorotica and Elysia timida rely specifically on algal energy production for development, growth, and reproduction. Elysia timida has also been shown to produce more eggs in the presence of light than in darkness. This amazing animal does not encode any algal genes in its nuclear genome. However, an apparatus of molecular mechanisms has evolved to respond, cope with, and maintain symbiosis with the stolen chloroplasts. Even though E. chlorotica needs to feed on Vaucheria litorea for one week before it reaches permanent kleptoplasty; after this, the slug becomes resistant to limited food access, which is an advantage since its main habitat is coastal marsh environments where the presence of Vaucheria sp. is sporadic. E.chlorotica can be found in the North East Atlantic.