Solar powered sea slugs: Is it all in the plastid?

Dec 19 2013 Published by under [Biology&Environment]

ResearchBlogging.org

Anyone who has followed this blog over the years knows that I have a bit of a thing for photosynthetic sea slugs. It's a complex story that has been worked on by several labs over a few years, and it is still not clear exactly what is going on. In short, there is a group of sea slugs that have the ability to feed on algae, and rather than digest their plastids (chloroplasts), the slugs store them in a reticulated intestine. Once full, the slugs stop feeding and apparently use the photosynthate produced by the plastids for several months. The catch, and why this is so interesting, is that plastids require proteins that are incoded in the nucleus of the alga. The sea slug digests the nucleus. So how does it work?

In 2008 evidence was published suggesting the slug had acquired nuclear genes from the alga. In 2010 I blogged about a study that countered this claim. In 2011 the story took a twist and it looked like the gene transfer story was an artefact. In 2012 the pendulum swung back and more data came out suggesting that ~60 algal genes reside in the sea slug nucleus.

What to make of all this? de Vries et al. have a different take and the secret may have been in the plastid all along.

The biggest hurdle that orphaned plastids have to deal with is degradation of the D1 protein of photosystem II. Most plastids we are familiar with require proteins that are encoded in the nucleus to be shuttled to the plastid in order to maintain the D1 protein. The plastids sequestered by sea slugs are divorced from their nucleus and the proteins it encodes. Therefore, they either have to be self-reliant to repair their photosystems or must rely on the host sea slug.

de Vries et al. suggest that the robust gene complement of plastids taken up by the sea slugs is directly responsible for their retention. Specifically, they site ftsH as instrumental in repairing the D1 protein of PSII. In many photosynthetic organisms, this protein is nuclear-encoded, but it remains in the plastids of the sea slugs' preference. In the absence of a nuclear contribution from the sea slug, the plastid may be able to repair itself for the lifespan of captivity in the slug.

Certainly this story is not over. This most recent paper even cites an "in press" manuscript that appears to demonstrate that the plastids are maintained in the slug for months in the dark, raising additional questions about how the slugs are utilizing the plastids. There have also been complications in the story based on different labs using different species of slugs (and their preferred algal food source) to ask the same questions. However, as this story continues to evolve the complex association between the slugs and the plastids they steal is slowly coming into focus.

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

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

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

de Vries J, Habicht J, Woehle C, Changjie H, Christa G, Wägele H, Nickelsen J, Martin WF, & Gould SB (2013). Is ftsH the key to plastid longevity in sacoglossan slugs? Genome biology and evolution PMID: 24336424

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