Sea slugs stealing more than plastids

Jun 14 2012 Published by under [Biology&Environment]
I've been fascinated by the story of the Elysia sea slugs for some time and have blogged about it before. In 2010 I covered the first paper with decent molecular evidence of a gene transfer from an alga to a sea slug and a follow up study. Earlier this year a number of papers came out with some new twists and recently I saw another chapter in story by Pierce et al (2012) has made it to print.

Elysia chlorotica (source)

If this story is unfamiliar you can read all the background in the two previous posts linked above, but this system appears to be very unusual. Essentially the sea slug hijacks the plastds (chloroplasts) from an alga and keeps them functioning for nearly a year. The plastids are the only parts of the alga maintained by the slug and once they are established, the slug no longer feeds. Not a big deal except for the fact that plastids need thousands of proteins that are encoded in the algal nucleus and targeted to function in the plastid. Where do those proteins come from when the algal nucleus is gone?

For years people have believed that the answer lies in the sea slug nucleus. If genes of algal origin were currently encoded in the sea slug nuclei, then the animal might be able to keep the plastids going. One complication is the need for a protein targeting system to get the slug-manufactured proteins to the plastids that need them. In their native alga, four membranes separate the plastid lumen from the cytoplasm. It is not clear how many membranes remain around the plastids once the sea slugs have ingested them, but a 5' "targeting signal" on the unfolded peptide and a number of chaperonins are typically required for it to arrive at the intended destination. Thus, it is not as easy as just acquiring a couple of novel genes.

A simplified diagram of gene transfer and targeting back to the plastid. (source)

In order to identify algal genes in the sea slug, Pierce et al. (2012) took a circuitous route. First they sequenced the genome and transcriptome of the alga the sea slug feeds on, Vaucheria litorea. This was done to produce an as-complete-as-possible algal protein set. Next, they sequenced the transcriptome of adult sea slugs with plastids, starved for 2 months. The idea here is to ensure that no algal contamination should be present, just the hijacked plastids and whatever the sea slug is using to keep them active. At this point, it was a simple comparison: are there any algal genes in the sea slug transcriptome?

The first thing they discovered is that the plastids are transcriptionally active. Transcripts from genes encoded in the plastid were identified, indicating that the plastid is making proteins. Why is this important? Because the plastid can't make proteins without some help from the nucleus. Plastids do not encode a complete set of genes for the machinery to carry out protein synthesis.

Next, they scanned the slug for transcripts that could not be traced back to the plastid genome and found 52 hits for algal genes among the slug transcriptome. Many of these (27) represented genes with functions related to photosynthesis and carbon fixation, with the remaining having unknown function. Interestingly, all of the putatively algal transcripts found in the sea slug transcriptome were in very low copy number and most did not overlap. This is in strong contrast to typical plastid-targeted transcripts, which can be some of the most abundant in actively photosynthesizing cells.

Additionally, many of the transcripts had a small number of nucleotide changes (1-6bp), when compared to the algal copy. Is this an indication that they are indeed encoded in the sea slug genome and their sequence is drifting from that of the alga? Perhaps.

After a several paragraph bashing of papers I previously covered here the authors conclude that the sea slug Elyssia chlorotica nucleus contains at least 60 genes that have been stolen from its algal prey. It uses these genes to supply proteins to the hijacked plastid for their continued function, albeit in low transcript abundance. The sea slug genome is underway and nearly finished, so the story may reveal yet further surprises.

Pierce, S., Fang, X., Schwartz, J., Jiang, X., Zhao, W., Curtis, N., Kocot, K., Yang, B., & Wang, J. (2012). Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Molecular Biology and Evolution DOI: 10.1093/molbev/msr316

10 responses so far

  • Scientist mother says:

    So cool!!!

  • Zuska says:

    OMG that is some freaking cool science!

  • becca says:

    Too much parenting. I think my brain is the approximate consistency of sea slug, because my first though (after ZOMG HOW COOL) was:

  • proflikesubstance says:

    Awwww, Maaaaannnn!

  • brooksphd says:

    That is fuckingamazing! Fuckshitdamn science is AWESOME!

  • Northern_Mockingbird says:

    Crafty Gene transfer & lovely little sea slug as a result!

  • Isabel says:

    The problem with transfer of genes with a multicellular animal would seem to be that the genes have to be transferred to the nuclei of the gametes, no? I can't see how this could happen.

    Also, weird how they used any old "algal" sequence to localize the Vaucheria genes- except for the diatom, most listed are probably no more closely related to Vaucheria (at one time a plastid thief itself) than they are to Elysia!

  • proflikesubstance says:

    Isabel - There are half a dozen other genomes done in that group, including the Ectocarpus and Aurecoccus genomes, which are quite close to Vaucheria. The reason to use more distantly related genomes is to take advantage of ones that are better characterized than the "non-models" that are more closely related.

    As for the gamete question, yes, one of the main barriers to eukaryotic gene transfer in complex organisms is the need to get into the germ line. While this is hardly the only example of it happening, it is clearly more difficult to accomplish than simply inserting into any cell's DNA.

  • Isabel says:

    Oh I forgot Ectocarpus was a brown alga. I knew there had to be closer genomes than all those greens.

    Still can't imagine how those gametes pick up the genes. Maybe in the environment? If they're living in a forest of constantly degrading Vaucheria, and the eggs and sperm are released there in great numbers...

  • Tanai says:

    Hi, I enjoyed your blogpost. Do you know where I can find some information about the genome of Elysia? I've been trying to look for the status of the genome but found nothing.
    All the best, Tanai.

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