The weird genome of water bears (tardigrades): more than a sixth of it swiped from distantly related species

Your eyes are growing heavy; you are growing sleepy; and now you WILL read this post!

Tardigrades, or “water bears,” are some of the world’s weirdest—and toughest—animals. They’re so bizarre that they constitute their own phylum, Tardigrada, but are related to arthropods and nematodes (roundworms), with whom—along with a few other beasts—they’re grouped in the “clade” Ecdysozoa.

Although they’re small, tardigrades are also very cute, and this photo shows why they’re called “water bears” (they’re also called “moss piglets” because of their snouts and frequent occupation of damp moss):

Source: American Museum of Natural History

Here’s a video of what they look like bopping around in the water:

What’s most remarkable about tardigrades is their toughness, which Matthew describes below. Wikipedia also notes this:

Tardigrades are notable for being perhaps the most durable of known organisms; they are able to survive extreme conditions that would be rapidly fatal to nearly all other known life forms. They can withstand temperatures from just above absolute zero [JAC: they can survive at -272°C, one degree above absolute zero] to well above the boiling point of water (100 °C) [JAC: they can survive at 151°C!], pressures about six times greater than those found in the deepest ocean trenches, ionizing radiation at doses hundreds of times higher than the lethal dose for a human, and the vacuum of outer space. They can go without food or water for more than 10 years, drying out to the point where they are 3% or less water, only to rehydrate, forage, and reproduce. They are not considered extremophilic because they are not adapted to exploit these conditions. This means that their chances of dying increase the longer they are exposed to the extreme environments, whereas true extremophiles thrive in a physically or geochemically extreme environment that would harm most other organisms.

If we ever destroy the planet with nuclear weapons, and only one form of life remains, it will not be cockroaches but tardigrades.

As we’ll see, their ability to dry out and then revive after rehydration may explain the remarkable result given in the paper I’ll describe today.  First, though, Matthew Cobb, who knows a lot about tardigrades (he lectures on them) volunteered to supply us with some Fun Tardigrade facts, below:

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Fun Tardigrade Facts (by Matthew Cobb)

• There are over 1000 species, all which are aquatic. They mainly live in terrestrial water-films, although one order is classed as ‘marine’ as it lives on the edge of the sea.

• They are disappointingly small: 0.05 – 1mm in length.

• They have four pairs of appendages, which are lobopod-like legs. They have a layered cuticle which appears to be chitinous, and grow by moulting, shedding their skin through their mouth opening.

• They are not arthropods, and although their bodies have indentations, they are not segmented. They belong in their own phylum, Tardigrada (named by Spallanzani in 1777, the word means ‘slow-stepper’), and are thought to be the closest relatives of Onychophora (velvet worms) and Arthropoda.

• They are a very ancient lineage – their ancestor separated from the ancestor of the arthropods over 700 million years ago. Some tardigrade lineages split around 630 million years ago, before the Ediacaran period, which is generally seen as being the first moment that multicellular organisms appear in the fossil record.

• Some of them are detritivores (i.e. they eat crap), others are carnivorous, eating rotifers and similar prey.

• They show a variety of modes of reproduction: sexual, parthenogenetic and even self-fertilisation in some hermaphroditic species.

• The weirdest thing is that during tough times they can shrivel up into what is called a ‘tun’ – a cold-resistant winter form. They do this by losing all but around 3% of their body water. This effectively turns them into something like a seed or a spore – alive, but only just, with minimal respiration (hence the technical term ‘cryptobiosis’). Just add water, and you revive the little beast. Here’s a scanning electron micrograph of a tun:

• In the tun state, tardigrades can resist temperatures as high as +149 C and as low -272ºC. You can immerse them in alcohol or ether, and they will still recover.

• In 2008, the TARDIS project (‘Tardigrades in space’) shoved some of these beasts on the outside of the Foton 3 satellite. There they were, whizzing round the planet in the hard vacuum and -272ºC in low Earth orbit for 10 days, holding onto the satellite as though their lives depending on it (NB artistic license here – they were in a box, in the tun state). When they were returned to Earth, tardigrades that had been exposed to space could be revived with the same frequency as control tardigrades. About the only thing that would kill them was if they were also exposed to all the electromagnetic radiation that bombarded the satellite. However, if they were protected from UV A and B rays, then about 15% of the tuns could initially be revived.

To learn more, including access to virtually every paper ever published on tardigrades, go to the delightfully retro Tardigrade Newsletter site. You’ll party like it’s 1999.

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JAC: What I want to highlight today is a new paper in the Proceedings of the National Academy of Sciences by Thomas Boothby et al. (reference and free link below; see also the summary on Science Alert). The upshot is that they sequenced the DNA of one species of tardigrade, Hypsibius dujardini, and found—astoundingly—that more than one-sixth of its genome, 17.5%, was from completely unrelated species—mostly bacteria. (This is the proportion of all genes coming from non-tardigrade species). This is nearly twice the proportion seen in the species previously known to have the most foreign genes: the rotifer Adinata ricciae (9.6% of its genes of foreign origin).

Here’s an individual of H. dujardini:

I’ll try to be brief here, though the results are truly astounding. In fact, you could consider them a dramatically new expansion of evolutionary theory, for they show that organisms can evolve not just via mutations in their own DNA, but by taking in genes from completely unrelated species.

Although we already knew this from studies of aphids, rotifers, and bacteria—the phenomenon known as “horizontal gene transfer” (HGT) has been described for some time—we had no idea that so much of a species’ genome could comprise genes taken from distant relatives. Although this doesn’t drastically change evolutionary theory (one could consider the uptake of these genes as a form of drastic “macromutation”), it does show that adaptations can in some cases evolve very quickly, and that these might (but usually don’t) screw up the branching phylogenetic trees that depend on assuming evolutionary change within lineages and no cross-lineage “genetic pollution.”

The authors simply sequenced the tardigrade genome (it didn’t used to be so simple!), and compared the sequence with the database of genes from other groups. They found that, as I said, about 17.5% of the tardigrade’s genes had their closest sequence match in completely unrelated species. The authors did controls, of course, to be sure that the DNA really was in the H. dujardini genome rather than being a contaminant from bacteria in the lab or in the tardigrade’s gut, and also to be sure that the foreign genes weren’t simply something that had been in the ancestor of the tardigrades and the putative source species, and was later lost in tardigrades. Everything was copacetic: all the genes were really taken in from distant species and incorporated into the H. dujardini genome.

Here’s the proportion of genes sequenced that came from different sources (note that they didn’t have data on 31.5% of the genes, so the 17.5% foreign-gene figure may well be an undestimate). The vast majority of genes acquired by HGT came from bacteria, with some from viruses, fungi, plants, and archaea:

 

(From paper):: Source of genes in the H. dujardini genome as determined by HGT index calculations following Galaxy tools taxonomy extraction

Some other results:

• Is the retention of foreign genes random? The kinds of foreign genes taken in were not random: they tended to be those involved in stress resistance, like heat-shock proteins, immune response genes (catalase genes), and genes producing proteins involved in DNA repair and protection of membranes. This makes sense, for tardigrades regularly undergo desiccation and rehydration in the wild, and when this happens their systems are shocked, their membranes stressed, and their DNA tends to fragment. The selective uptake of genes, then, suggests that there has been natural selection on the tardigrades to take in foreign genes that protect them from and help them recover from stress.

• How does the horizontal gene transfer occur? When tardigrades dry out, losing 97% of their body water, and then rehydrate, they take in water from the environment, and that water may contain foreign DNA. We also know that the tardigrade nuclear membrane becomes porous when this occurs, so that foreign DNA could enter the nucleus and integrate into the species’ genome. After that, natural selection would occur, with those animals having foreign genes that help them survive this process leaving more offspring. In that sense it’s pretty normal natural selection, but with the “mutations” comprising absorbed DNA from distantly-related taxa rather than coming from random errors in the tardigrade’s own DNA.

• Have the foreign genes evolved since being taken into the tardigrade genome? Yes, certainly. The sequences are different from those in bactria, and in tardigrades they’ve also evolved “introns” (spacer DNA that separates parts of a single gene, which is present in tardigrades and other eukaryotes but not bacteria). Further, the “codon usage”—the particular triplets used to code for an amino acid—have also changed to correspond more closely to the frequency of usage in tardigrades than in the source bacteria. So after the foreign genes were incorporated and spread by natural selection, a more conventional process of natural selection tweaked the sequences of those foreign genes.

Now the million-dollar questions:

How common is this phenomenon, and does it tend to occur in certain types of species? While geneticists have found other cases of HGT, and it seems to take place in rotifers as well as at least this species of tardigrade, it doesn’t seem to be so common as to overwhelm the genomes of most species. For if it were that common, we simply wouldn’t be able to make credible evolutionary trees (“phylogenies”)—trees that depend critically on assuming that genetic change occurs by mutations within lineages, not by the wholesale movement of DNA among diverse lineages. Because trees are usually easy to construct, and don’t show signs of much HGT, we can be pretty confident that this phenomenon does not take place often in most species. (Bacteria, however, undergo HGT more often, making it harder to construct bacterial phylogenies.)

As for why it occurs in rotifers and this tardigrade (researchers need to look at more tardigrade species to see if H. dujardini is exceptional), there are two theories. One is that the absorption of foreign DNA is an adaptive response to the absence of sexual reproduction—a way to get genetic diversity in the absence of being able to swap genes among members of your own species. The authors discount this because, although this species includes mostly females who reproduce parthenogenetically (without sex), males are known to occur and the species does undergo reduction division, or meiosis. Also, there don’t seem to be special mechanisms that have evolved for taking in DNA. Rather, that DNA absorption appears to be a byproduct of what happens when tardigrades dry out and rehydrate, being stressed in the process.

I tend to go along with the authors’ theory that HGT in this species is simply a byproduct of what happens when tardigrades dry out—one aspect of cryptobiosis, a form of metabolic shutdown that occurs when organisms dehydrate, freeze, or are subject to other stress. In the case of tardigrades, I noted that this breaks their DNA and injures their membranes. When they rehydrate, they could take in some genes from foreign species that would help them repair their DNA and overcome their stress. Those foreign genes that aided in this survival would be those that get passed on. That’s natural selection.

To test this idea, we need to sequence the DNA of other species that undergo crytobiosis and rehydration, organisms like the brine shrimp (Artemia salina). One would predict that HGT would be more common in such species. In fact, the brine shrimp genome might already have been sequenced, although I can’t find any reports on it. If it hasn’t, scientists should get off their butts, sequence it, and look for evidence of HGT.

Finally, how much does this affect our view of evolution? As I said, although this doesn’t overturn the conventional theory of evolution by natural selection, it does expand it in two ways. First, we have to realize that “mutations” can include more than slight tweaks in an organism’s genome due to errors in replication, exposure to radiation, and so on. There can be “macromutations” in which a whole new gene is suddenly spliced into your genome. But after that happens, evolution will proceed as it always does: if the macromutations are adaptive, they’ll spread by natural selection; if they have no effect on the organism’s fitness (i.e., they’re “neutral”), they’ll be subject to the random sampling of genetic drift; and if they’re deleterious, natural selection will weed them out.

Second, if HGT were common and pervasive, it would make it hard to judge how organisms were related, which we do by making phylogenetic trees. Such trees would be hard to make if HGT were frequent, for trees are, as I said, based on the assumption that each lineage changes by mutation, drift, and selection in its own DNA, not by taking up foreign DNA from very unrelated species. The fact that such trees are usually made in eukaryotes without evidence of HGT suggests that HGT is not so common as to overwhelm the normal accumulation of genetic change within lineages. In this view of life, what we have is an amazing and unexpected phenomenon, one never conceived of by either Darwin or his immediate successors. It’s a view that expands our understanding of how evolution works but that doesn’t produce a new “evolutionary paradigm.”

You might recall that when HGT was found in bacteria and a few other species, New Scientist published an infamous edition with this cover claiming that DARWIN WAS WRONG:

He was supposedly wrong because the tree of life, so the article said, was based on the palpably false assumption that there was no movement of genes among distantly-related. Well, that’s not the case, and New Scientist simply suffered from Kuhn Envy. Darwin wasn’t wrong. He was mostly right, but didn’t anticipate something that could occasionally but rarely complicate the making of trees.

h/t: jsp

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Boothby, T. C., J. R. Tenlen, F. W. Smith, J. R. Wang, K. A. Patanella, E. Osborne Nishimura, S. C. Tintori, Q. Li, C. D. Jones, M. Yandell, D. N. Messina, J. Glasscock, and B. Goldstein. 2015. Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proceedings of the National Academy of Sciences. Published online before printNovember 23, 2015, doi:10.1073/pnas.1510461112

Jönsson, KI, Rabbow, E., Schill, R.O., Harms-Ringdahl, M. and Rettberg, P (2008) Tardigrades survive exposure to space in low Earth orbit. Current Biology 18:R729–R731