Friday, May 09, 2008

Is DNA Repair A Substitute For Sex?

Yeah, it's a trick question. The answer is clearly "no" – unless you're a bdelloid rotifer.

What's interesting, of course, about these minute but multi-cellular animals is that they are completely asexual, and apparently have been for millions of years. There are no males, and females reproduce entirely by parthenogenesis. Although that might seem to imply a rather joyless existence, it hasn't stopped the bdelloids from persisting, and even diversifying into more than 370 species.

The conventional evolutionary reason for the invention and predominance of sexual reproduction – apart from the recreational aspect – is that it provides a mechanism for a species to cope with the inevitability of sustaining damage to its DNA. So why do the bdelloids seem to think they have a better way?

Is DNA Repair A Substitute For Sex?
These hardy creatures somehow escape the usual drawback of asexuality – extinction – and the MBL’s David Mark Welch, Matthew Meselson, and their colleagues are finding out how.

In two related papers published recently in Proceedings of the National Academy of Sciences (PNAS), the team proposes an interesting hypothesis: Bdelloid rotifers have been able to give up sex and survive because they have evolved an extraordinary efficient mechanism for repairing harmful mutations to their DNA. ...

In animals that do have sex, DNA repair is accomplished during meiosis, when chromosomes pair up (one from the father, one from the mother) and “fit” genes on one chromosome can serve as templates to repair damaged genes on the other chromosome. The bdelloid, though, always seems to reproduce asexually, by making a clone of itself. How then, does it cope with deleterious mutations?

Before we come to the hypothesized answer, it must be noted that the bdelloids' ability to repair their DNA is not merely adequate. It's spectacularly good:
MBL adjunct scientist Matthew Meselson and Eugene Gladyshev, both of Harvard University, demonstrate the enormous DNA repair capacity of bdelloid rotifers by zapping them with ionizing radiation (gamma rays), which has the effect of shattering its DNA into many pieces. “We kept exposing them to more and more radiation, and they didn’t die and they didn’t die and they didn’t die,” says Mark Welch. Even at five times the levels of radiation that all other animals are known to endure, the bdelloids were able to continue reproducing.

“Because there is no source of such intense ionizing radiation on Earth, except if we make it, there is no way these organisms could have evolved to be radiation resistant,” says Mark Welch. Instead, they propose that bdelloids’ DNA repair capacity evolved due to a different environmental adaptation – tolerance of extreme dryness.

Bdelloids, which live in ephemeral aquatic habitats such as temporary freshwater pools and on mosses, are able to survive complete desiccation (drying out) at any stage of their life cycle. They just curl up and go dormant for weeks, months, or years, and when water becomes available, they spring back to life. Mark Welch and his colleagues showed that desiccation, like ionizing radiation, breaks up the rotifers’ DNA into many pieces. Presumably, the same mechanisms they use to survive desiccation as part of their life cycle also protect them from ionizing radiation.

Hmmmm. That sounds oddly familiar. Where have we heard about that sort of thing before? Oh yes, this is apparently exactly the same thing found in a bacterium (Deinococcus radiodurans), as discussed here. And in the closely related bacterial species, Deinococcus geothermalis, as discussed here.

But what the bdelloids do is much more impressive, since they are multicellular eukaryotes, not simple prokaryotic bacteria. In any case, what't the trick for bdelloids?
One feature that may confer exceptional DNA repair capacity on the bdelloids is described in the team’s second PNAS paper. Here, they give evidence that the bdelloid rotifer, like most animals, originally had two copies of each chromosome. But at some point in its evolution, it underwent a “whole-genome duplication,” giving it four copies of each chromosome and hence of each gene. Normally, lineages that undergo whole-genome duplication lose the duplicate genes over time. The bdelloid, though, has kept most of its duplicate genes throughout its evolutionary history.

“We believe they have kept most of their duplicate genes because they are serving as templates for DNA repair,” says Mark Welch.

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