Tiny tunicate throws structure to the wind
Today I bring you something extra special: A guest post from Lucas Brouwers of the world-famous blog Thoughtomics. He loves genomes, I love plankton, and you get a great story involving spaceships, genomic party crashers, and, of course, a planktonic sea squirt. Enjoy!
Just below the surface of the sea, little animals are floating through a universe where the stars are made of plankton. They travel in what can best be described as gelatinous spaceships, which provide both shelter and food. They are Oikopleura dioica (Oikos is ancient Greek for house or household).
Their spaceships are ingenious constructions, made in such a way that every beat of Oikopleura‘s tail brings in a new flow water. The water and all the plankton it contains, is led through different tubings and chambers of the ship, until it reaches the waiting mouths of Oikopleura. The spaceships are not of a durable design and last for only a couple of hours before they are broken down again. Oikopleura spend the largest part of their short lives (5-10 days) repeating a cycle of building, feeding and destruction.
As small and short-lived as they may be, their genomes are evolving at at an extraordinary speed. A large team of scientists sequenced the full genome of Oikopleura recently, and found that its genome has been reorganized and trimmed down on an unprecedented scale.
One of the first things they noticed was the rapid evolution of introns in the genes of Oikopleura. Introns are the genetic equivalent of party crashers who show up at parties uninvited. They hang around inside genes, without coding for anything. Our cell have to force the introns out of messenger RNAs before they can properly be translated into proteins. Despite their apparent lack of use, many genes of distantly related animals have introns in exactly the same places. These introns have been conserved for millions of years, leading some to believe that they provide an evolutionary advantage somehow.
Oikopleura doesn’t care about these million year old traditions though. A staggering 76,2% (or 4.260) of its introns are unique to Oikopleura. Conversely, 3.917 of introns that are present in other animals (including close relatives) have been lost in Oikopleura. Not only do the newer introns outnumber their older peers, they are also good deal shorter than the few introns that have been retained.
But the extensive remodeling of the genome didn’t stop with introns. Normally, genes tend to hang out in similar neighborhoods in different species. There’s a good chance that two genes that are close to one another in mouse, are also close together in the human genome for example. Just like introns, many of these neighborhood relationships have persisted in species that are as far apart as humans and sponges.
Not so in Oikopleura. Its genes have been shuffled and switched around until the point that conventional gene orders are no longer recognizable. For small sets of genes the gene order in Oikopleura is closer to random than the gene order in other species.
The authors subtly hint at a potential cause for all this genetic upheaval: Oikopleura‘s genome lacks a full set of DNA repair genes. DNA is a robust molecule, but it can still be damaged. One of the nastier things that can happen is that both DNA strands of a single chromosome break. Cells can repair this type of damage in two different ways. The first way of repair works by taking a close look at the sister chromosome, and see how the damaged strands should be repaired, as shown in the video below. Another way is to directly seal the broken ends.
Oikopleura is lacking the genes for this last type of repair work. This means that every double strand break in Oikopleura‘s DNA can only be repaired via a sister chromosome, increasing the recombination rates (the exchange of genetic material between chromosomes) for Oikopleura. The causal link between the missing DNA repair genes and the accelerated evolution of Oikopleura‘s genome remains to be proven, but it isn’t hard to imagine how their absence could have played a large role in the overhaul of genomic architecture.
In addition to having a fast evolving genome, Oikopleura also has one of the smallest animal genomes (70 MB, compared to 3,174 MB for humans), which still contains some 18,000 genes (compared to ~21,000 in humans). Clearly, we don’t need that extra 3,100 MB for only a couple of thousand genes more. Compared to Oikopleura, our genomes are like attics crammed full of boxes and old furniture. Some scientists think that many features of our genomes (such as introns) are quite unnecessary, while others disagree. The debate boils down to this: are we keeping all the stuff because it is worth a lot, or because we never got around to throwing all the junk away?
Since Oikopleura was successful in redecorating and cleaning out its entire genome, our conserved genomic architecture might be nothing more than a product of historical contingency. In the small and slowly reproducing human population, natural selection might not be strong enough to remove all the unnecessary junk.
Despite the large genomic changes, Oikopleura has remained an animal in every way. While it might not be immediately obvious, they are very closely related to us vertebrates (animals that carry a backbone such as fish, reptiles, birds and mammals). They don’t have a spine, but they do have a lining of tough cells (a notochord) and a neural tube running through their entire bodies.
Oikopleura belongs to a group of animals known as tunicates, or sea squirts. Most sea squirts live a sedentary life on the ocean floor where they filter plankton from seawater. They are basically hollow bags with two siphons – one for drawing seawater in, and the other to expel waste and water. But the solitary and free swimming Oikopleura don’t look anything like these stationary creatures, so what are these familial ties based on?
A different life stage holds the answer: every sea squirt starts its life as a larvae, looking very much like Oikopleura. After swimming around for a couple of days the larvae attach themselves to a comfortable looking outcropping and morph into the sedentary sea squirts. By retaining its larval features and delaying its further development, the ancestor of Oikopleura has permanently avoided the fate of settling down (these processes are known as neoteny and progenesis).
The similarity between vertebrates and sea squirt larvae implies that our own vertebrate ancestor once looked very much like larvaceans such as Oikopleura. Like Oikopleura, we are basically sea squirts that have never grown up. But unlike them, we still carry the baggage of 600 million years of animal evolution. I think there is much that we can still learn from the Peter Pans of the oceans.
Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C, Brinkmann H, Mikhaleva J, Olsen LC, Jubin C, Cañestro C, Bouquet JM, Danks G, Poulain J, Campsteijn C, Adamski M, Cross I, Yadetie F, Muffato M, Louis A, Butcher S, Tsagkogeorga G, Konrad A, Singh S, Jensen MF, Cong EH, Eikeseth-Otteraa H, Noel B, Anthouard V, Porcel BM, Kachouri-Lafond R, Nishino A, Ugolini M, Chourrout P, Nishida H, Aasland R, Huzurbazar S, Westhof E, Delsuc F, Lehrach H, Reinhardt R, Weissenbach J, Roy SW, Artiguenave F, Postlethwait JH, Manak JR, Thompson EM, Jaillon O, Du Pasquier L, Boudinot P, Liberles DA, Volff JN, Philippe H, Lenhard B, Crollius HR, Wincker P, & Chourrout D (2010). Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate. Science (New York, N.Y.) PMID: 21097902