In the mosses and lichens of the world – the in-between places, where living conditions rapidly fluctuate – lives a tiny animal with an extraordinary survival skill.
No, not tardigrades – it's their much weirder housemate, the bdelloid rotifer.
Just like tardigrades, bdelloid rotifers can dry out almost completely and spring back to life when water returns. They can be blasted with radiation hundreds of times greater than what would kill a human, and live to tell the tale, even while their chromosomes are shattered.
And now, scientists have discovered, one bdelloid rotifer can do something never before documented in any other living organism, even tardigrades: A species called Adineta vaga can reproduce without putting its chromosomes back together after radiation damage – and its offspring will continue fixing the damage over generations.
"What's really exceptional in this discovery is that somehow they stabilize the ends of the chromosome; they stabilize these DNA pieces, and then they can transmit it to the next generation and then continue the repair," evolutionary biologist Karine Van Doninck of the Université Libre de Bruxelles in Belgium told ScienceAlert.
"That's never been shown, that you have this repair across generations."
The discovery started with an earlier experiment – and a signal so unexpected that the researchers thought something must have gone awry.
The team had subjected A. vaga to powerful radiation, collected an egg laid by one of the animals, and used that egg to establish a clonal population.
Because all those clones originated from the same egg, the researchers expected to see the same radiation damage reflected across their genomes.
Instead, they found something strange. Large deletions in the chromosomes varied between individuals, and the sequencing data seemed to show the missing DNA being progressively restored.
"It suggested a progressive repair, and we thought that's impossible," Van Doninck said.
At first, the researchers suspected the problem may have lain in the sequencing. But when they repeated their analyses, the strange pattern stubbornly remained.
The ragged edges of the deletions provided an important clue: They were not the same between individuals, suggesting that after the chromosomes broke, the exposed DNA had continued to degrade – but to different extents in different individuals – before the repair process began.
Over the following months, the researchers continued tracking the damaged genomes through successive generations, using DNA sequencing and chromosome counts to work out what they were seeing.
Gradually, the team realized what was taking place. The rotifers weren't repairing much of the chromosome damage before reproducing. Broken chromosome fragments were surviving into the next generation, where the repair process could continue.
"Indeed, this was totally unexpected, and it took us some time to figure out what was happening, and we really had to pinch ourselves to believe it," molecular biologist Bernard Hallet of the Université Catholique de Louvain in Belgium told ScienceAlert.
It was no minor damage, either.
The researchers exposed A. vaga to proton radiation at doses of 100, 250, and 500 grays, estimated to inflict around 88, 220, and 440 double-strand DNA breaks across the genome, respectively.
At the highest dose, an individual chromosome could be shattered into as many as 30 to 50 pieces.
Ordinarily, this poses a pretty big problem. During cell division, including the meiosis that produces reproductive cells, chromosomes rely on a region called the centromere to drag the necessary genetic material into the new cell. Without the centromere, the daughter cell cannot receive that fragment.
A. vaga, however, appears to have found a loophole.
"Our results suggest that, in contrast, Bdelloid rotifer chromosomes have a 'holocentric' structure with key structural components of the centromere being spread along separate regions across the chromosome – which ensures that chromosome fragments containing these components can be segregated properly," Hallet explained.
That means that when a chromosome shatters, its fragments may still retain what they need to be pulled into a daughter cell – allowing the broken pieces to persist across cell divisions and, ultimately, generations.
But that's only half of its remarkable trick. The other half is the repair itself.
A. vaga has a diploid genome, meaning its chromosomes come in pairs. The two chromosomes in each pair are homologous – they carry the same genes in the same locations, although the precise versions of those genes can differ.
That gives a damaged chromosome something extremely useful: a relatively intact 'twin' it can use as a repair template.
Although the rotifer reproduces asexually, it has retained an unusual form of meiosis in which those homologous chromosomes pair up. A broken DNA end can therefore seek out the matching region on its intact homolog and use that sequence to reconstruct what has been lost.
The researchers call the mechanism break-induced homologous extension repair, or BIHER.
If the damage is severe enough, that repair takes multiple rounds – that is, successive generations of rotifers all chipping away at the problem. But here's the truly extraordinary thing: The findings suggest that, eventually, the damaged chromosome can be completely repaired.
"Our results indeed show that reiterative BIHER can potentially restore the original structure of a broken chromosome, with some deletions being completely eliminated after a certain number of generations," Hallet said.
"In other words, given sufficient time, the missing sequence can be progressively restored."
At this point, you may quite naturally be wondering what on Earth A. vaga is doing in its leisure time that it needs such a potent defense against ionizing radiation.
Well, the answer to that has to do with its mossy habitat.
Mosses and lichens can dry out for long periods before becoming wet again, and their tiny inhabitants have had to evolve ways to survive those extremes. Bdelloid rotifers (and tardigrades, actually) do this by entering a state of almost complete desiccation – drying out like it's an extreme sport.
Drying out, however, is extraordinarily hard on DNA. It can cause the same kinds of physical damage as ionizing radiation, including the double-strand breaks that can shatter chromosomes.
So A. vaga probably didn't evolve its extraordinary repair abilities in response to radiation at all. Its radiation resistance appears to be a fortuitous side effect of adapting to survive repeated bouts of desiccation.
"The physical damage of desiccation is by chance the same as radiation, and so they became radiation resistant," Van Doninck explained. "That's the beauty of nature."
And that ability to survive while its genome is in an utter omnishambles could make A. vaga useful for understanding other situations in which chromosomes undergo catastrophic damage.
On Mars, for example, human explorers will likely experience radiation doses considered dangerous for humans. And cancer cells can experience a phenomenon called chromothripsis, in which chromosomes shatter and are stitched back together in dramatically rearranged forms.
"Sometimes I say rotifer is like a living cancer, so it's a very interesting model system for all this research," Van Doninck said.
There are still questions to answer. The researchers now want to better understand the molecular machinery that allows A. vaga to pull off its extraordinary repairs, and whether similar strategies might be hiding elsewhere in nature.
Related: These Tiny Creatures Were Revived After 24,000 Years Frozen in The Siberian Permafrost
Van Doninck also noted that the team is now investigating what happens when both homologous chromosomes are broken at the same location, leaving the rotifer without the intact template BIHER normally relies on – and we're somewhat agog to find out, too.
This is a tiny microscopic creature that is probably living in your backyard – and yet it has this remarkable self-repair superpower that could teach us something about survival in the most extreme circumstances. That's extraordinary.
"The concept of transgenerational transmission and repair of broken chromosomes was totally unexpected," Hallet said.
"I consider it as one of the nicest discoveries of my career."
The findings have been published in Science Advances.
This article was fact-checked by Michael Irving and edited by Michael Irving. While we pride ourselves on our process, we are only human. If you spot a mistake, please let us know.