Solar Sea Slugs: Part animal, part plant... or not?

Original image here.

(Update here)

Sea slugs are far more interesting than their name might imply. Aside from being beautiful, they have some unusual ways of making a living. In the case of a few unrelated species, they steal for a living.

A handful of sea slugs have found away to make the most of the algae they eat. As they take in the cellular contents of the algae, they are able to separate the components and isolate the light harvesting organelles, the plastids. Whereas the majority of the chewed algal is digested, the plastids are spread throughout the specialized digestive track of the slugs so that they form a layer all over the upper part of the slug, giving it a green color. Depending on the species of slug, the animal can then rely entirely on the plastids for weeks to months as the sole source of energy, making them the solar powered slugs.

Elysia chlorotica feed on algae and then steal the plastids to harness solar energy.

But here is where the story gets interesting. It is well documented that plastids have high protein turn-over, especially in their light harvesting complexes. The constant barrage of photons breaks the antenna proteins down and they need to be constantly replaced. Those proteins, however, are not produced by genes encoded on the genome of the plastid. Instead, they are nucleus-encoded and targeted to the plastid by the cell cytosol, thanks to a signature extension on the 5' end of the transcript. Therefore, the algal nucleus is essential for the continued maintenance of functional plastids. But the slugs sequester ONLY the plastids, no nuclei. How do the slugs keep the plastids going for months in the absence of the algal nuclei and the essential plastid proteins they produce?

In 2008, it appeared that there might be an answer. Rumpho et al (2008) looked at the genome of E. chlorotica and identified genes that appeared to be derived from the algal nucleus. Gene transfer from the nucleus of an algal to that of an animal for the purpose of allowing the slug to maintain its own plastids! Needless to say, this story got a lot of press. The only issue was, there were very few genes found, and none of the major antenna proteins one would expect must be there. But it was a PCR-based survey, not a genome sequence, so people reasoned that the genes were there, just not PCR friendly for whatever reason.

Not so fast, claim Wägele et al. in an article released yesterday in Molecular Biology and Evolution. Wägele et al. sequenced cDNA from two slug species made from RNA transcripts (genes being expressed by the animal) extracted from plastid-containing slugs that were kept without a food source, and were thus entirely dependent on the plastids for carbon. Based on the findings of Rumpho et al. (2008), the expectation would be that genes encoded in the slug nucleus that had been transfered there from the alga for the purpose of plastid maintenance would be highly expressed under these conditions. Afterall, the plastids are actively photosynthesizing for the slug and have to deal with the wear and tear of the job.

But contrary to expectation, Wägele et al. found NO evidence of the antenna proteins, the Calvin cycle enzymes or the small subunit of RuBisCO (which is absent from the plastid of the algae the collected slugs were feeding on). This means that the plastids have no back-up proteins - once a protein that can not be made by the plastid breaks down, that's it. Based on what we know about plastids, this should happen within a matter of days - without a constant stream of new proteins from the nucleus, the photosynthetic apparatus should cease to work.

But that is NOT what we observe in the sea slugs. They maintain functional plastids for MONTHS. One explanation is that transcript levels of these critical proteins were too low for detection, but this is an entirely unsatisfying conclusion because 1) Next generation sequencing was used to produce very deep coverage of the transcripts, and 2) the small subunit of RuBisCO alone, accounts for roughly 15% of all transcripts in young plant leaves. The probability of missing all of the transcript necessary for the plastids to survive is virtually nil.

So what is going on? The answer, I'm afraid, is elusive. What we see in nature can not be explained by what we know about the components of the system. The proteins are not being made by the slug and the plastids can not survive as long as they do without replacement proteins, or so our current knowledge would suggest. Something has to give to explain our observations and I'm am eager to see what it is. With the E. chlorotica genome soon to be completed, answers may be on the horizon... or not.

References:
Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, & Manhart JR (2008). Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences of the United States of America, 105 (46), 17867-71 PMID: 19004808

Wagele, H., Deusch, O., Handeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S., Dagan, T., Klussmann-Kolb, A., & Martin, W. (2010). Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobrachus ocellatus does not entail lateral transfer of algal nuclear genes Molecular Biology and Evolution DOI: 10.1093/molbev/msq239