The Solar Sea Slug story gets.... odd(er)

Aug 25 2011 Published by under [Biology&Environment]

ResearchBlogging.org

I've followed the scientific developments surrounding the fascinating kleptoplasty of sea slugs for a while, mainly because it's an intriguing riddle. How does an animal steal plastids (chloroplasts) from an alga and keep them alive for 9+ months, all in the absence of the algal nucleus?

If you are unfamiliar with the story, go check out this first post of the topic from a few months ago. As a quick primer, however, certain sea slugs suck out the contents of algae, then digest everything but the plastids. They then sequester these plastids in their articulated gut and can survive solely on the energy provided by the organelles for months. This might not be that surprising, except for the fact that the genomes of plastids only encode about 1/10 of the proteins required for their function. The remaining proteins are encoded in the nucleus of the algae and directed to the plastids via a protein targeting pathway. So if the sea slugs keep only the plastids, where do 9/10 of the necessary proteins come from?

In 2008, this system looked like a possible case of large scale DNA transfer from the algal nucleus to that of the sea slug when an algal gene was identified from the nucleus of the sea slug, Elyssia chlorotica (Rumpho et al. 2008). However, subsequent work by Wagele et al (2011) found no evidence of transfer in related sea slugs that show similar behavior. At the time the response was "Well, maybe gene transfer is specific to E. chlorotica", so transcriptome studies were launched on this beast.

But now the results are trickling in and the story has taken an odd twist. Deep sequencing of the E. chlorotica genome not only fails to reveal any strong evidence of active algal genes in photosynthesizing sea slugs, but none of the algal genes previously identified as putative transfers are detected (Pelletreau et al. 2011, Rumpho et al. 2011). So what is going on?

Although the 2011 Pelletreau and Rumpho papers claim that horizontal gene transfer (HGT) can not yet be ruled out, the probability of algal genes playing a central role in this kleptoplasty is beginning to look highly unlikely. Sure, it is possible that those genes follow different expression patterns than we would expect, but the facts are that the plastids still need to function and the proteins need to come from somewhere. There is no protein fairy that replaces critical cofactors and enzymes in the middle of the night. If we can't detect the mRNA, it is highly unlikely that the nucleus is harboring the genes of interest.

That leaves us having to consider alternatives to traditional cell biology, which is fascinating in it's own right. Are the sea slugs using enzymes to store the proteins in the gut, releasing them to the plastids as needed? Are there protein-stabilizing properties of the sea slug gut? If so, how does the slug recognize the plastid-targeted proteins while digesting the rest? Another curious aspect of the story is that the plastids consumed by the sea slug are typically encased in four membranes, but the outer two are digested away by the slug, possibly simplifying the protein delivery system. This also has implications for the original HGT hypothesis because if the sea slug nucleus acquires genes that have targeting peptides for four membranes, they may not be processed correctly when only two membranes remain.

When this system was first descibed there were many questions. The HGT story in 2008 made it appear as though there might be an incredible adaptation that give rise to kleptoplasty, but in the last year the story has once again become muddled as new data have failed to support the HGT hypothesis. IMO, genomics alone is not going to solve this one. Someone is going to have to get freaky with some protein isolation work and figure out what is going on in the gut, and where. As a non-model system with no genome sequence, it is not clear when this will happen, but my guess is that the answer will be worth the work.

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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

Wägele H, Deusch O, Händeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussmann-Kolb A, & Martin W (2011). Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Molecular biology and evolution, 28 (1), 699-706 PMID: 20829345

Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, & Rumpho ME (2011). Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant physiology, 155 (4), 1561-5 PMID: 21346171

Rumpho ME, Pelletreau KN, Moustafa A, & Bhattacharya D (2011). The making of a photosynthetic animal. The Journal of experimental biology, 214 (Pt 2), 303-11 PMID: 21177950

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