Solar-powered green sea slug steals ability to photosynthesise from algae

edyong — Sun, 28 Dec 2008 11:00:55 +0000

Solar power is a relatively new development for humans but, of course, many living things have been exploiting the power of the sun for millions of years, through the process of photosynthesis. This ability is usually limited to plants, algae and bacteria, but one unique animal can do it too - the emerald green sea slug Elysia chlorotica. This remarkable creature steals the genes and photosynthetic factories of a type of algae that it eats (Vaucheria littorea), so that it can independently draw energy from the sun. Through genetic thievery, it has become a solar-powered animal and a beautifully green one at that.

The cells of algae, like those of plants, contain small compartments called chloroplasts that are its engines of photosynthesis. As the Elysia munches on algae, it takes their chloroplasts into the cells of its own digestive system, where they provide it with energy and sugars. It's a nifty trick that provides the sea slug with an extra energy source, but the problem is that it shouldn't work.

Chloroplasts are not independent modules that can be easily separated from their host cell and implanted into another. They are the remnants of once-independent bacteria that formed such a strong alliance with the cells of ancient plants and algae, that they eventually lost their autonomy and became an integral part of their partner. In doing so, they transferred the majority of their own genes to their host so that today, chloroplasts only have a tiny and depleted genome of their own, containing just 10% of the genes it needs for a free-living existence.

So, shoving a chloroplast from an algal cell into an animal one should be about as effective as installing a piece of specialised Mac software on a PC. The two simply shouldn't be compatible, and yet Elysia and its chloroplasts clearly are. Mary Rumpho from the University of Maine discovered the key to the partnership - the sea slug has also stolen vital genes from the algae that allows it to use the borrowed chloroplast. It has found a way to patch its own genome to make it photosynthesis-compatible.

The pilfered gene is called psbO and it codes for a protein called MSP (manganese-stabilizing protein, in full). MSP is so important to the chemical reactions of photosynthesis that it is found in all species that have this ability, with very few differences between the various versions.

The pbsO gene has never before been spotted in an animal genome, but Rumpho found it amidst the sea slug's genes. To make sure that she wasn't just detecting undigested algae that had been left over in the slug's body, Rumpho also searched for pbsO in the DNA of sea slug eggs that had never been previously exposed to algae. She found it there too - clearly, the gene had been fully assimilated into the slug's own genome.

There is no doubt as to its origin - it must have come from the algae for both the slug's pbsO gene, and the MSP protein it codes for, were exact matches for the versions carried by V.littorea. Rumpho also found that other genes involved in photosynthesis have been transferred from the algae to the slug. This is a vital point for without these genes, the stolen chloroplasts wouldn't work. The slug itself is providing the proteins that make photosynthesis possible.

Elysia's antics are that much more intriguing because gene-swapping of this sort is very rare outside the bacterial world. Bacteria trade genes like humans swap gossip and on rare occasions, they will transfer genes (or even their entire genomes) into the more complex cells of animals and plants. And there are even fewer examples of genetic trade between these 'higher' kingdoms, which makes the tale of the slug and the algae all the more extraordinary.

We can only speculate about the route that led to Elysia wielding algal genes, but Rumpho has an idea. She suggests that once upon a time, swallowed algae ruptured in the gut of a sea slug, setting free its DNA, which was then taken up by the cells of the animal's digestive system. Somehow, this absorbed DNA was incorporated into Elysia's own genome.

In an email exchange with Carl Zimmer, Rumpho notes that Elysia's digestive system branches very closely to its sexual organs, giving the absorbed DNA a route into the animal's sex cells, and from there, into the next generation. She also notes that the sea slugs are almost always infected with a virus, which could act as a vehicle that shuttles DNA from destroyed algae into slug cells.

The story of Elysia and its genetic kleptomania is yet another example of animals undergoing the sort of horizontal gene transfer that is so commonplace in bacteria (see my previous posts on Space Invaders and rotifers). With similar reports growing in number, we would be foolish to underestimate the importance of such transfers in animal evolution.

Reference: M. E. Rumpho, J. M. Worful, J. Lee, K. Kannan, M. S. Tyler, D. Bhattacharya, A. Moustafa, J. R. Manhart (2008). From the Cover: Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica Proceedings of the National Academy of Sciences, 105 (46), 17867-17871 DOI: 10.1073/pnas.0804968105

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edyong Sun, 12/28/2008 - 06:00

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horizontal gene transfer

Very cool. Further evidence that molluscs are the pinnacle of all creation ;)

That is totally fucking cool! Any idea how long ago the gene transfer is thought to have occurred?

I wonder, given enough time, if these slugs could evolve a method to directly transmit the chloroplasts themselves from one generation to the next, and thus, eventually lose their digestive system, becoming full-time photosynthesizers?

Matt, you risk inflaming the infamous ScienceBlog Invertebrate Wars again. But yes, molluscs are awesome - definitely much cooler than echinoderms... ;-)

PP, paper doesn't give any clues unfortunately. I'm assuming that no related species of sea slug has the same ability, so I would guess since Elysia chlorotica diverged from its closest relative, whenever that was. I don't really know how you'd go about narrowing it down further - if pbsO is such a highly conserved gene anyway, it's unlikely that it would have changed much since being transferred, so doing a cross-individual phylogeny wouldn't help matters much. Perhaps our geneticist colleagues can pitch in?

Assuming anyone coming here knows, but how is it the chloroplasts, being an organelle, are actually moved into the cells? I wouldn't imagine it's common for objects of that size to permeate the cell membrane.

I read about this a little while back and was just fascinated by it. An interesting experiment would be to try and get a group of these slugs to uptake some other gene, see if we could reverse engineer the process. I recall using GUS genes as a marker in plant experiments, so I assume a similar item could be used for slugs.

Some other species of the genus Elysia also have symbiotic algae, such as Elysia viridis and Elysia crispata. The gene transfer may be a primitive characteristic of a sacoglossan ancestor; it would also be interesting if it evolved multiple times.

Actually, I see that the page on Sacoglossa has a link to a forum that specializes on sea-slugs, which page on algal chloroplast usage states that in addition to many sacoglossans using the trick, many nudibranches absorb and enter into symbiotic relationships with whole cells (as opposed to just the organelles like chloroplasts).

Assuming anyone coming here knows, but how is it the chloroplasts, being an organelle, are actually moved into the cells? I wouldn't imagine it's common for objects of that size to permeate the cell membrane.

I don't know the answer, but I did find a report that might have some fascinating implications about the symbiotic relationship between all eukaryotic cells and their organelles.

Uptake of Isolated Chloroplasts by Mammalian Cells
http://www.sciencemag.org/cgi/content/abstract/165/3898/1128

I would tentatively suggest that cells can uptake organelles from very foreign species precisely because there is an ancient common coordination mechanism among all eukaryotes and their organelles, dating back to the earliest eukaryote-prokaryote symbiosis.

If you Google for the article title, and follow the link for scholar.google.com, there are more papers on the topic of cells and organelle uptake and symbiosis.

You have to wonder how often such transfers happen. If they're not so rare, in a few thousand years one of these slugs might similarly steal the ability to actually generate its own chloroplasts.

Moreover, what evolutionary path would such a slug follow. It could conceivably lend quite an advantage to an organism...

It may not be exactly analogous, but DNA moves between organelle and nucleus much more freely than is usually assumed.

Sadly guys, there is no Southern blot evidence for this 'gene transfer'. I'm afraid this looks more like a case of PCR contamination.................. much like a recent similar paper published in the journal symbiosis by Pierce et al., which also did not have southern blot data.

how can the gene be there without a southern blot?????????

Don't believe everything you read, even in PNAS......!

Actually, the paper says there's Northen blot evidence.

I'm not a biologist (I write novels!) but this gave me shivers. Beautiful.

Look closely at the northern blot for Elysia. This is typical of northern blots conducted at low stringency - the hybridization is NON-SPECIFIC. look at the signal to noise ratio on the Elysia lane - its terrible. why is this not seen on the Vaucheria lane? if I were to use a probe from a gene from say potato, and use this against human total RNA at low stringency, this is what I would get (eg 42oC, as described in the methods). this would not be evidence that human DNA contains genes from potato. the banding likely corresponds to rRNA and is essentially background.

sorry

Wow....and this adaptation isn´t related to the nudibranch ability of take on entire nematocysts from cnidarians?

I've featured E. crispata (which as noted does a similar thing) a couple of times on my tuesday nudi slot:
http://tai-haku.blogspot.com/2007/02/tuesday-nudi.html
http://tai-haku.blogspot.com/2008/07/tuesday-nudi.html
Elysia are very cool slugs.

Thanks for this wonderful post.

Wow, that's really interesting stuff. I had no idea sea slugs could do that. It's almost kind of creepy :)