Sex and the Rotifer

Bethany: I'm sorry. Sex is a joke in heaven?
The Metatron: The way I understand it, it generally is down here as well.

--Scene from the movie Dogma

Gladyshev, E. A., M. Meselson & I. R. Arkhipova. 2008. Massive horizontal gene transfer in bdelloid rotifers. Science 320 (5880): 1210-1213.

Nature has an annoying, almost pathological, tendency to break her own rules (I think it may have been Terry Pratchett who commented, "There's a reason why nature is called a mother"). Just when we biologists think we've got it all sorted out, something new comes along to mess up the theory. And, of course, nothing gets more complicated than sex. Sex, one would think, is a good thing - as well as its obvious immediate attractions, it serves to mix up the gene pool and increase variety in the population, increasing the chances for survival in a changing world. And yet many organisms do without it. How?

Most authorities who have given thought to the subject have concluded that asexually reproducing organisms survive on an "if it ain't broke, don't fix it" principle. After all, sexual reproduction can be a complicated, energy-sapping buiness, and if the individual is already well-suited to its environment, then the best option is to bypass the issue entirely. The resulting hypothesis is that asexual reproduction works better in the short term by preserving the parent's advantages, but sexual reproduction works better in the long term, as changing circumstances increase the chance of prior advantages becoming less so. Indeed, many organisms capable of asexual reproduction, such as aphids, support this hypothesis by acting in a manner that seems geared to extract the best from both options - reproducing asexually so long as conditions remain good, then switching to sexual reproduction when conditions deteriorate.

But remember what I said about nature breaking its own rules? Bdelloid rotifers are the prime exception in this case. Despite being estimated to have diverged from other animals some 80 million years ago, bdelloids are entirely asexual. How, the question runs, have they been able to survive so long without some form of genetic recombination? A paper in today's Science suggests how - by incorporating genes from other organisms. In a study of transposable elements (TEs - pieces of DNA that are able to move about in the genome) in the bdelloid Adineta vaga, Gladyshev et al. unexpectedly found that many of the TEs actually contained protein-coding sequences. What is more, analysis of these coding sequences found that many of them were not similar to genes found in other animals. Instead, the bdelloid genes clustered with bacteria, fungi or even plants.


A bdelloid rotifer, probably Philodina acuticornis. Photo by Aydin Örstan.

Horizontal gene transfer (HGT) is the transfer of genetic material from one organism to another by non-reproductive means. This may occur through genetic material being carried by viruses, for instance, or by direct transfer. The occurrence of HGT in bacteria has been established beyond a doubt, and most researchers regard it as a significant factor in bacterial evolution. Whether (or to what degree) it occurs in eukaryotes has been a far more contentious subject*. A certain degree of HGT has been demonstrated in flowering plants (Bergthorsson et al., 2003; Nickrent et al., 2004 - one of my earlier posts touched on a probable case of HGT to a parasitic plant from its host). Animals, however, are regarded as much less prone to HGT, but bdelloids seem to be an exception once again.

*There is one notable class of exceptions. Many of the eukaryote organelles (such as mitochondria and chloroplasts) have been derived from endosymbiotic bacteria, and one component of their conversion from independent organisms capable of living freely to obligate endosymbionts has been large-scale HGT from the endosymbiotic bacterium to the nucleus of the host eukaryote. Let it suffice to say for now that the candidate HGT-derived genes in bdelloids do not appear to have been derived from this route.

The reason why animals are so resistent to HGT, and the main problem with recognising its occurrence in bdelloids, is that there are less apparent methods for foreign genetic material to be transferred into animal cells (there is also the separation in most animals between the somatic and reproductive cells). Bacteria are able to transfer genetic material between each other by the productive of pili, tubular structures that latch onto other cells. Plants lack pili, but they do possess plasmodesmata, openings in the cell wall that allow for the transport of materials between adjoining cells, and it is possible that HGT can occur via the plasmodesmata when plants of two different species grow in contact with each other (this may be how the host-parasite transfer mentioned earlier occurred, for instance). Animals, on the other hand, lack both pili and plasmodesmata. If the HGT-candidate genes in bdelloids really are such, their means of entry remains entirely hypothetical. Viral transfer is one possibility, but would require that bdelloids be somehow more prone to viral infection than other animals. Gladyshev et al. point tentatively at the unusual life history traits of bdelloids as a possible solution. Bdelloids are able to survive extreme dessication, and Gladyshev et al. suggest that damage to cellular membranes in the course of dessication might increase their chance of taking up foreign genetic material. Also, the authors found no cases where the specific source of an HGT-candidate was identifiable, though this could merely represent evolutionary change in the time since assimilation.

What is also interesting is that the HGT-candidate genes were not randomly distributed in the bdelloid genome. Most were concentrated in parts of the genome separate from more standard animal genes, closer to telomeres in areas rich in TEs. The authors suggest (quite reasonably, I think) that this results from the greater potential for interference with pre-existing genetic processes were horizontally transferred genes to insert in functional sectors of the genome. (Note that this is not necessarily to say that HGT products don't become inserted in these sectors, but that most of those cells that did experience such an insertion would not remain viable.) As already referred to, many of the HGT-candidate genes seem to have undergone significant change since their insertion, and a few of the genes that appear to have been derived from bacteria have themselves actually had introns (characteristic of animals, but generally absent from bacteria) inserted into them.

If bdelloids are indeed so amoenable to HGT, this could go some way to explaining their ability to cope without sexual reproduction, as HGT supplies another potential method for genetic recombination. It would be of great interest to see whether other microscopic animals that often undergo dessication cycles, such as tardigrades, also show elevated HGT rates, as this may be informative in testing whether it is the bdelloids' life cycle that has made them so accepting.

REFERENCES

Bergthorsson, U., K. L. Adams, B. Thomason & J. D. Palmer. 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197-201.

Nickrent, D. L., A. Blarer, Y.-L. Qiu & R. Vidal-Russell. 2004. Phylogenetic inference in Rafflesiales: The influence of rate heterogeneity and horizontal gene transfer. BMC Evolutionary Biology 4: 40.