Solar-Powered Sea Slugs

 Placida dendritica on Codium fragile. Photo credit: Seth Goodnight

 Placida dendritica on Codium fragile. Photo credit: Seth Goodnight

I'm going to tell you about a fantastic little group of gastropods called sacoglossans. They are the subject of my PhD work, as well as my Master’s thesis. I’m pretty sure that by the end of this post you’ll agree with me that they are pretty amazing. First, I’ll give you a little background information.

Sacoclossans are herbivorous sea slugs that feed by sucking the cell sap out of algae. I call them a group (or a clade, if you prefer) because there is some disagreement about whether Sacoglossa is an order or a sub-order... possibly an infra-order... maybe a super-family. I'm getting off topic here. I'll write a post about why I hate taxonomy some other time. You’re here to read about sea slugs.  Almost every species feeds on green algae, and most of the food species are coenocytic (basically algae that are comprised of one giant cell). There are several exceptions (as is always the case in biology) including: Elysia catulus (which eats eelgrass), E. evelinae (which eats diatoms), Calliopaea oophagea (which eats sea slug eggs), and at least half a dozen others that similarly varied diets (Jensen 1980).

International kleptoplasty champion (2000-2013): Elysia chlorotica . Photo credit: Patrick Krug Cataloging Diversity in the Sacoglossa LifeDesk. Wikimedia Commons

International kleptoplasty champion (2000-2013): Elysia chlorotica . Photo credit: Patrick Krug Cataloging Diversity in the Sacoglossa LifeDesk. Wikimedia Commons

What do you mean by "solar-powered"?

The most exciting and fascinating part about the sacoglossans (certainly the thing that got me interested) is that some of them can actually become photosynthetic. That's right, animals that gain energy from sunlight. As they extract the cell sap, they are able to separate the chloroplasts and absorb them into the cells lining their digestive tracts (Trench et al. 1969); this is a process termed kleptoplasty (“klepto-“ as in stealing, and “-plasty” referring to plastids like chloroplasts). The exact mechanism used to separate the chloroplasts is still a mystery, but many people think that it's similar to how many nudibranchs (a different clade of sea slugs) are able to sequester stinging cells from corals and anemones that they eat. While not every species can make use of ingested chloroplasts, some are able to live exclusively on sunlight, at least temporarily. Elysia chlorotica is the current record holder and is able to live for up to nine months on just sunlight (Rumpho et al. 2000).

Lots of animals have symbiotic algae, what makes sacoglossans so special?

For one thing, sacoglossans don't have symbiotic algae; they are actually taking only the chloroplasts and digesting the rest. This process is well known from single celled organisms, but sacoglossans are the only animals that do so. Furthermore, the chloroplasts aren't passed on from one generation to the next, nor are they present in the larvae. The slugs will not be able to gain chloroplasts until they metamorphose and begin feeding as juveniles and adults. 

Placida dendritica : Notice the green trails throughout the body. That is the shape of the digestive tract. Photo credit: Seth Goodnight

Placida dendritica : Notice the green trails throughout the body. That is the shape of the digestive tract. Photo credit: Seth Goodnight

How did such a process evolve?

As with all questions about evolution, there are no certain answers, but I've read one very plausible explanation. Sacoglossans are small soft-bodied animals with very few defensive mechanisms. Holding on to the chloroplasts gives the slugs the same pigments that the algae has, making them very hard to see (Jensen 1997). They have a highly branched digestive tract that spreads the pigment evenly throughout the animal's body. Since the animals were already gaining some benefit from keeping the chloroplasts intact and the chloroplasts are able to retain their function outside of their host cell the slugs eventually started to gain energy from sunlight (Giles and Sarafis 1971). The branched digestive tract aided in exposing more chloroplasts to the sunlight. At some point, genes from the algal nucleus were transferred to the nucleus of the animal (at least in the case of Elysia chlorotica), meaning that they can synthesize proteins necessary to maintain chloroplasts (Rumpho et al. 2008).

This is exactly the kind of thing that gets me jazzed about biology. Here you have these sea slugs that have adapted a great form of camouflage, and then they become photosynthetic as a result. Here's something else to think about: Chloroplasts were most likely free-living organisms (cyanobacteria) at one time.  They were ingested by early eukaryotes, and eventually became organelles (giving rise to the first algae). Now they are being consumed and absorbed by animals, and are taking the first evolutionary steps towards becoming permanent organelles in animals. Life has a wonderful way of breaking all of the rules that we humans try to prescribe to it.

 

Here's a great video of a juvenile Elysia chlorotica feeding for the first time.

 

References

Giles, K. L. and V. Sarafis. 1971. On the survival and reproduction of chloroplasts outside the cell.

Cytobios 4:61-74.

Jensen, K. R. 1980. A review of sacoglossan diets, with comparative notes on radular and buccal 

anatomy. Malacological Review 13:55-77.

Jensen, K. R. 1997. Evolution of the Sacoglossa (Mollusca, Opisthobranchia) and the ecological 

associations with their food plants. Evolutionary Ecology 11:301-335.

Rumpho, M. E., E. J. Summer, and J. R. Manhart. 2000. Solar-powered sea slugs. Mollusc/algal 

chloroplast symbiosis. Plant Physiology 123:29-38.

Rumpho, M. E., J. M. Worful, J. Lee, K. Kannan, M. S. Tyler, D. Bhattacharya, A. Moustafa, and J. R. 

Manhart. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic 

sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences 105:17867-17871.

Trench, R. K., R. W. Greene, and B. G. Bystrom. 1969. Chloroplasts as functional organelles in animal 

tissues. The Journal of Cell Biology 42:404-417.