Elysia and Other Photosynthetic Sea Slugs

Elysia is an “opisthobranch” sea slug famous on the internet for its remarkable ability to photosynthesise, giving it the nickname of “solar-powered sea slug”. It does this by kleptoplasty – stealing plastids from its algal food. If you note the greenish colour in E. asbecki above (Wägele et al., 2010), the green comes from the harvested chloroplasts. This post will look at this process, and generally at the biology of the genus.

Before starting, it’s worth noting that while Elysia is the most famous of these examples on the internet, it’s definitely not the only animal that can photosynthesise by symbiosis with algae. Falkowski & Knoll (2007) have a three page-long table (pp. 90-92) listing various eukaryotes where this has been documented, including sponges, corals, ascidians, flatworms, and bivalves.

E. chlorotica, if internet fame is anything to go by, is probably the poster child for the phenomenon, and also the one that exhibits it the best. It can harvest the chloroplasts from any number of ulvophycean and xanthophyte algae, but the most successful relationship is with the xanthophyte alga, Vaucheria litorea. The chloroplasts get sequestered intracellularly in the digestive epithelium, and stay functional for over 14 months (Rumpho et al., 2006). This isn’t just an opportunistic relationship, but one that has evolved into a real symbiosis, as evidenced by the identification of lateral transfer of V. litorea nuclear genes into the E. chlorotica genome (Schwartz et al., 2010), most tellingly the transfer of the oxygenic photosynthesis gene, psbO, and fcp, associated with light-harvesting complexes (Rumpho et al., 2008). This is also the reason why naming it a symbiosis may be a mistake, as it doesn’t involve two genetically independent organisms (Law & Lewis, 1983). Nomenclature aside, the chloroplast is hugely beneficial for the slug, as it provides “free” carbohydrates at times when food isn’t available (e.g. in winter, when host algae don’t grow).

Interestingly, the algal chloroplast loses its host membrane and outer two of the four chloroplast membranes (Rumpho et al., 2000) and is found free-living in the cytoplasm in adults after getting phagocytosed (Rumpho et al., 2000). In juveniles, they are bound within a special membrane.

Elysia contains over 120 species, accounting for ~40% of all sacoglossans. In fact, the phenomenon was first discovered in E. atroviridis, not E. chlorotica (Kawaguti & Yamasu, 1965), with functionality of chloroplasts documented by Taylor (1967) and evidence that the chloroplasts contribute to the animal’s metabolism by Trench et al. (1972). Other Elysia species do not nearly have E. chlorotica‘s efficiency, with most retaining the chloroplast for a couple of months at best, after which the chloroplasts degrade and get enveloped in phagosomes and presumably digested (Marín & Ros, 1993). Feeding allows chloroplasts to get replaced, but this is limited by the presence of algae. It is however notable that chloroplasts from multiple species can get sequestered (Curtis et al., 2006), so it’s not necessarily a specific interaction.

Elysia belongs to the Plakobranchidae, a family where long-term plastid retention is autapomorphic (Händeler et al., 2009) and lasts over a couple of weeks generally, but outside of the family, the association lasts for no more than a week. Individuals behaviourally try to control light intensity in order to maximise the lifespan of the inherited chloroplasts and to regulate photosynthesis rate (Casalduero & Muniain, 2008), but at some point, the chloroplasts just stop working.

A very valid question to ask is how such an association can arise. The ability to acquire plastids from food is most probably an ancestral one in sacoglossans, and is linked to one of the main autapomorphies of the Sacoglossa, a radula with only one row of teeth and one median tooth (Mikkelsen, 1996; pictured above from E. asbecki from Wägele et al. (2010)), which is what allows the animal to pierce the algal cell and suck out the plastids (Jensen, 1997). This is a feeding style that is highly-specialised and not found anywhere else in the molluscs, and underlies the reason why sacoglossans feed only on septate and siphonous algae, with only some also feeding additionally on other plants such as seagrass (Jensen, 1981). Each species, depending on their specificity, can also have further modifications to fit the radula perfectly to its host plant (Jensen, 1994), and it’s likely that host shifts can play a role in diversification and speciation, as hinted at by Trowbridge & Todd (2001)‘s work on the shifting of a Scottish subpopulation of E. viridis to feeding on an invasive alga within the past 50 years.

The retention of plastids can be imagined as having considerable fitness benefits, for example a free food source in the winter when algae don’t grow, or conferring a defensive adantage as camouflage – once they ingest the chloroplasts, the slugs turn green, identical to the background, and this is a tremendous advantage considering their lack of shell. There is also some evidence that their food gives them defensive compounds to sequester as well as chloroplasts, for example chlorodesmin, a fish repellent (Hay et al., 1989).

On to Elysia‘s general biology. The monophyly of the genus is not known for sure, and is strongly supported only by molecular phylogenies (Händeler et al., 2009). Truly diagnostic macroscopic features are not to be found, as is clear from field guides, where sacoglossans are all lumped together as unidentified morphospecies. So if you happen to catch one (your best bet is to look carefully in algal meadows, at any depth, keeping in mind that they will be well-camouflaged), your best bet is to consult an expert or trawl through seaslugforum.net.

As all gastropods, Elysia mating involves “love darts”. Schmitt et al. (2007) describe the process in E. timida, where it basically amounts to a synchronised shooting of hypodermic love darts, followed by a short period of standard vaginal impregnation aided by glandular fluids. You can view3 videos from that paper here. Elysia‘s life cycle involves a planktonic larval stage, with the veliger larva having a sinistral shell and dispersing for a couple of weeks or more. The metamorphosis to the adult takes place when the veliger attaches itself to a film of microorganisms growing in an alga-rich habitat.

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References:

Casalduero FG & Muniain C. 2008. The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. Journal of Experimental Marine Biology and Ecology 357, 181-187.

Curtis NE, Massey SE & Pierce SK. 2006. The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebrate Biology 125, 336-345.

Falkowski PG & Knoll AH. 2007. Evolution of primary producers in the sea.

Green BJ, Li W-J, Manhart JR, Fox TC, Summer EJ, Kennedy RA, Pierce SK & Rumpho ME. 2000. Mollusc-Algal Chloroplast Endosymbiosis. Photosynthesis, Thylakoid Protein Maintenance, and Chloroplast Gene Expression Continue for Many Months in the Absence of the Algal Nucleus. Plant Physiology 124, 331-342.

Händeler K, Grzymbowski YP, Krug PJ & Wägele H. 2009. Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life. Frontiers in Zoology 6, 28.

Hay ME, Pawlik JR, Duffy JE & Fenical W. 1989. Seaweed-herbivore-predator interactions: host-plant specialization reduces predation on small herbivores. Oecologia 81, 418-427.

Jensen KR. 1981. OBSERVATIONS ON FEEDING METHODS IN SOME FLORIDA ASCOGLOSSANS. Journal of Molluscan Studies 47, 190-199.

Jensen KR. 1993. Morphological adaptations and plasticity of radular teeth of the Sacoglossa (= Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biological Journal of the Linnean Society 48, 135-155.

Jensen K. 1997. Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological associations with their food plants. Evolutionary Ecology 11, 301-335.

Kawaguti S & Yamasu T. 1965. Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biological Journal of Okayama University 11, 57-65.

Law R & Lewis DH. 1983. Biotic environments and the maintenance of sex–some evidence from mutualistic symbioses. Biological Journal of the Linnean Society 20, 249-276.

Marín A & Ros J. 1993. ULTRASTRUCTURAL AND ECOLOGICAL ASPECTS OF THE DEVELOPMENT OF CHLOROPLAST RETENTION IN THE SACOGLOSSAN GASTROPOD ELYSIA TIMIDA. Journal of Molluscan Studies 59, 95-104.

Mikkelsen PM. 1996. The evolutionary relationships of Cephalaspidea s.l. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia 37, 375-442.

Rumpho ME, Summer EJ & Manhart JR. 2000. Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis. Plant Physiology 123, 29-38.

Rumpho ME, Dastoor FP, Manhart JR & Lee J. 2006. The Kleptoplast. Advances in Photosynthesis and Respiration 23, 451-473.

Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Chattacharya D, Moustafa A & Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. PNAS 105, 17867-17871.

Schmitt V, Anthes N & Michiels NK. 2007. Mating behaviour in the sea slug Elysia timida (Opisthobranchia, Sacoglossa): hypodermic injection, sperm transfer and balanced reciprocity. Frontiers in Zoology 4, 17.

Schwartz JA, Curtis NE & Pierce SK. 2010. Using Algal Transcriptome Sequences to Identify Transferred Genes in the Sea Slug, Elysia chlorotica. Evolutionary Biology 37, 29-37.

Taylor DL. 1967. THE OCCURRENCE AND SIGNIFICANCE OF ENDOSYMBIOTIC CHLOROPLASTS IN THE DIGESTIVE GLANDS OF HERBIVOROUS OPISTHOBRANCHS. Journal of Phycology 3, 234-235.

Trench RK, Trench ME & Muscatine L. 1972. Symbiotic Chloroplasts; Their Photosynthetic Products and Contribution to Mucus Synthesis in Two Marine Slugs. Biological Bulletin 142, 335-349.

Trowbridge CD & Todd CD. 2001. HOST-PLANT CHANGE IN MARINE SPECIALIST HERBIVORES: ASCOGLOSSAN SEA SLUGS ON INTRODUCED MACROALGAE. Ecological Monographs 71, 219-243.

Wägele H, Stemmer K, Burghardt I & Händeler K. 2010. Two new sacoglossan sea slug species (Opisthobranchia, Gastropoda): Ercolania annelyleorum sp. nov. (Limapontioidea) and Elysia asbecki sp. nov. (Plakobranchoidea), with notes on anatomy, histology and biology. Zootaxa 2676, 1-28.

Research Blogging necessities :)

Katharina Händeler1, Yvonne P Grzymbowski, Patrick J Krug, & Heike Wägele (2009). Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life Frontiers in Zoology DOI: 10.1186/1742-9994-6-28
Mary E. Rumpho, Elizabeth J. Summer, & James R. Manhart (2000). Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis Plant Physiology DOI: 10.1104/pp.123.1.29
Mary E. Rumpho, Farahad P. Dastoor, James R. Manhart, & Jungho Lee (2006). The Kleptoplast Advances in Photosynthesis and Respiration DOI: 10.1007/978-1-4020-4061-0_23

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