Space Invader DNA jumped across mammalian genomes

Blogging on Peer-Reviewed ResearchMammals like ourselves pass our genes 'vertically' from parent to child. But bacteria aren't quite so limited; they have mastered the art of gene-swapping and regularly transfer DNA 'horizontally' from one cell to another. This "horizontal gene transfer" has been largely viewed as a trademark of single-celled organisms, with few examples among animals and plants. That is, until now.

A group of American researchers have discovered a group of genetic sequences that have clearly jumped around the genomes of several mammals, one reptile and one amphibian. It's the most dramatic example yet that horizontal genetic transfer outside of the bacterial realm is more common than we thought, and has helped to shape the evolution of animals. Meet the Space Invaders, genetic hitchhikers coming soon to a genome near you.

John Pace from the University of Texas originally discovered the sequences he named Space Invaders (or SPIN elements) by looking at the genome of a small primate called a bushbaby. He was searching for transposons, a group of parasitic DNA sequences that can cut themselves out of genomes and jump to new locations of their own accord. One sequence in particular stood out and Pace searched for it in all other vertebrates whose full genomes have been sequenced.

To his surprise, he found a large number of matches among the DNA of seven very distantly related species - the green anole (a lizard), African clawed frog, little brown bat, mouse, rat, opossum and tenrec , a small animal that looks like a hedgehog but is more closely related to elephants, manatees and aardvarks.

i-3f15e95485d7fe022e0d4bf0a4fc28e8-SPINcarriers.jpg

While these animals come from very diverse lineages, their SPIN sequences were incredibly similar; compare those of any two species and you'd get an average match of 96%. That is a remarkable resemblance; even genes for some of the most vital, unchanging proteins within the vertebrate repertoire aren't that similar between different species.

The widespread but patchy distribution of SPIN sequences means that it is extremely unlikely that the seven species inherited these sequences from the same common ancestor. They each have close relatives with completely sequenced genomes that lack any SPINS; they're in tenrecs but not elephants, in mice and rats but not squirrels, and in bushbabies but not macaques or humans.

There is more evidence. None of the SPIN elements (except for those in the rat and mouse) were found at the same locations in their respective genomes. And while the Space Invaders, like all transposons of their ilk, have characteristic sequences at their ends, theirs all differ in a small but consistent way - a single change to their sequence that always shows up in the same position and sets them apart from other transposons.

It's strong evidence that they all of these species picked up their SPIN passengers independently. All the modern sequences are descended from a common ancestor, a transposon forefather that jumped across the genomes of all these species and left its descendents in its wake. They aren't closely related to any other transposons so they don't tell us the identity of the 'Patient Zero' species that was the source of the ancestral sequence, or how said sequence managed to jump into so many different vertebrates.

But Pace has some ideas on those fronts; he suggests that the Space Invaders may have infiltrated the genomes of vertebrates by stowing away aboard certain viruses. There is precedent for that - last year, scientists discovered a piece of DNA that hitched a ride from the genome of a carpet viper into that of a gerbil, by hitching a ride onboard a poxvirus that infected both species. And four of the species that harbour SPINs - bats, opossums, mice and rats - are rich reservoirs of poxviruses that could act as vehicles for mobile DNA.

Regardless of their origins, the SPINs have been busy in their new hosts. Each genome typically contains many copies of the full-length versions and even more shorter variants that do not have the ability to jump around themselves. Together, these short versions (known as MITEs) and the full-length originals can number in their thousands. The frog has 4,000 of them and the tenrec has around 99,000, making SPINs some of the most successful transposons known.  

In one case, within the genomes of mice and rats, a SPIN element appears to have given rise to a new gene. It's not clear what it does, but it appears to be functional and dates back to the time before mice and rats diverged from each other. But for the most part, natural selection has turned a blind eye to these sequences, and they have simply drifted through evolutionary time, picking up the odd neutral mutation.

Based on this steady drift, Pace estimated that the majority of SPINs spread through the genomes of vertebrates  between 31 and 46 million years ago, with a possible second burst about 15 million years ago that affected the bat and opossum. That's a very narrow period of time in evolutionary terms and during it, the elements managed to 'infect' the DNA of very unrelated species living in distant parts of the world. It was effectively a global pandemic that left lasting consequences.

Reference: J. K. Pace, C. Gilbert, M. S. Clark, C. Feschotte (2008). Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0806548105

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Too cool--thanks for this. The biogeography is interesting--the green anole's entire family is New World, whereas the frog and some of the mammals exclusively African in lineage.

By Sven DiMilo (not verified) on 03 Nov 2008 #permalink

I can't wait for the contortions and howlers from evolution-denying YECs, who will undoubtedly say that this is evidence for a front-loaded genome revealed by a series of'saltational events.'

Extremely interesting stuff, thanks!

Evolution has a microbial and environmental component, but its the later that gets all the attention and we intuitively use to describe it. What you describe highlights a more complex side to the story ... and frankly one I don't understand.

And in Tralfamadorian, it probably says "Help, I am being held prisoner in ...."

By Hank Roberts (not verified) on 03 Nov 2008 #permalink

Ed, when you say, "The frog has 4,000 of them and the tenrec has around 99,000", presumably you're talking about the elements rather than the base pairs from which they're composed, so just how many base pairs in total are we talking about here of these repetitive sequences?

Ian - good question. Yes, those numbers refer to the copy number. In terms of base pairs, it's quite a substantial amount. In the tenrec, they add up to about 67 Megabases (that's 67 million base pairs)!

Does this have any bearing on the utility of genetic modification? Sorry if this is a stupid question, it sounds as if it is a similar process, though happening in a very different way.

Many thanks Ed for this nice post. Very accurate.

Sven's right; to us too the biogeography of SPIN invasion is one of the most fascinating and intriguing aspects of the story. The presence of SPIN in opossum and Anole, both currently endemic to South/Central America and presumably already so at the time of the transfers (15-40 Mya), while the other species are either strictly restricted to Africa (tenrec, bushbaby) or have a broader geographic distribution (vesper bats, murine rodents) suggest that there was intercontinental and interoceanic movement of SPIN transposons, possibly via intermediate vector(s) such as bugs and/or viruses. Interestingly, phylogenetic analyses (not shown in the paper) are consistent with the geographic distribution, with the SPIN consensus sequences of the opossum and Anole (slightly) more closely related to each other than to the other species.

But it's important to keep in mind that we have looked so far at a very small sample of species, biased for the genome sequences that were available in the databases at the time of the study. We are currently investigating further this and other related questions with an experimental and more systematic approach. Stay tuned for more SPINs on the story!

I love it when scientists comment on posts based on their own work. I love it even more when said scientists make an amusing pun based on their own work :-)

Welcome Cedric and thanks for the update. Great stuff you're working on.

sounds like they're desperately trying to avoid special creation to me. "Miraculous space-invader jumping genes miraculous fling themselves across time and space." Uh-huh. Even if that is true, it's just another example of adaptation that doesn't involve natural selection being the cause. Anyone ever notice that RMNS is NEVER validated anywhere?

stan,

it's just another example of adaptation that doesn't involve natural selection

SPINs are not adaptations.

Anyone ever notice that RMNS is NEVER validated anywhere?

No, I never noticed that. Maybe you should talk to Richard Lenski about that.

sounds like they're desperately trying to avoid special creation to me

How does this support special creation at all? These sequences, with one exception, are not adaptive so there is no evidence of design here. If anything, the existence of non-adaptive (to the host organism) sequences are a powerful argument against special creation/intelligent design. The exception is a supposedly functional gene in Murines that is derived from a SPIN. If this sequence was specially created why would it be derived from a SPIN sequence rather than constructed de novo? Honestly, you creationist trolls. Sheesh.

"Miraculous space-invader jumping genes miraculous fling themselves across time and space." Hm... stan ignored the rules grammar as well as the whole bit about a possible mechanism via poxviruses.

and, PS: "it's just another example of adaptation that doesn't involve natural selection being the cause"

Not all changes in genome are from natural selection. Changes in allele frequencies, for example, can be due to chance - like if an avalanche were to suddenly wipe out every blonde-haired person in Switzerland. Suddenly everyone born there would have dark hair - but not by natural selection (which requires that the gene somehow relates to an individual's fitness). Natural selection isn't the only process of evolution...

I wonder if this is the same Stan who got chucked into Pharyngula's dungeon. Regardless, this is as good a time as any to mention my new policy on commenters. I only very rarely delete/censor comments. However, if you post something really stupid here, I will take that as implicit agreement that you are unconcerned about how you appear in public and are therefore happy for me to make you look even stupider. Click on Stan's name to see what I mean.