Bdelloid Rotifer *Adineta vaga* Repairs Broken Chromosomes Across Generations

In the mosses and lichens found around the world – those in-between environments where conditions can change rapidly – lives a minute animal with an exceptional survival ability.

It is not a tardigrade, but its far stranger neighbour: the bdelloid rotifer.

Like tardigrades, bdelloid rotifers can lose almost all their water and revive when moisture returns. They can also withstand radiation doses hundreds of times higher than those fatal to a human, surviving even when their chromosomes have been broken apart.

Scientists have now found that one bdelloid rotifer can achieve something never previously recorded in any other organism, including tardigrades. A species known as Adineta vaga can reproduce without first reassembling chromosomes damaged by radiation, while its descendants continue repairing that damage over successive 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."

How Adineta vaga repairs broken chromosomes across generations

The finding emerged from an earlier experiment, after the researchers encountered a result so surprising that they initially believed something had gone wrong.

The team exposed A. vaga to intense radiation, took an egg produced by one of the animals, and used it to create a clonal population.

Since every clone came from that single egg, the scientists expected the same radiation-induced damage to appear throughout all of their genomes.

Instead, they observed something unusual. Large chromosome deletions differed from one individual to another, while the sequencing results appeared to indicate that the absent DNA was gradually being restored.

"It suggested a progressive repair, and we thought that's impossible," Van Doninck said.

Initially, the researchers thought the sequencing itself might be at fault. Yet when they repeated the analyses, the unusual pattern persisted.

The uneven deletion edges offered a crucial clue. They varied between individuals, indicating that once chromosomes had broken, the exposed DNA kept degrading – though by different amounts in different rotifers – before repair began.

Over the next several months, the researchers followed these damaged genomes through consecutive generations. DNA sequencing and chromosome counts helped them determine what was happening.

Eventually, the team understood the process. The rotifers were not repairing most chromosome damage before reproduction. Instead, fragments of broken chromosomes survived into the following generation, where their restoration 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.

Nor was the damage insignificant.

The researchers subjected A. vaga to proton radiation doses of 100, 250, and 500 grays, calculated to cause approximately 88, 220, and 440 DNA double-strand breaks across the genome, respectively.

At the greatest dose, a single chromosome could be split into as many as 30 to 50 fragments.

Usually, that would create a major problem. When cells divide, including during the meiosis that creates reproductive cells, chromosomes depend on a region known as the centromere to pull the required genetic material into the new cell. A fragment without a centromere cannot be inherited by the daughter cell.

A. vaga, however, seems to have found a way around this limitation.

"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.

As a result, when a chromosome breaks apart, its fragments may still carry the components needed to be drawn into a daughter cell. This lets the broken pieces endure through cell divisions and eventually across generations.

BIHER gives the bdelloid rotifer a DNA repair template

That is only one half of the rotifer's extraordinary ability. The other is the repair process itself.

A. vaga possesses a diploid genome, which means that its chromosomes occur in pairs. The two members of each pair are homologous: they contain the same genes in the same positions, although the exact forms of those genes may vary.

This provides a damaged chromosome with something highly valuable: a comparatively undamaged 'twin' that can serve as a template for repair.

Although the rotifer reproduces asexually, it has retained an unusual type of meiosis during which homologous chromosome pairs come together. A broken DNA end can therefore locate the equivalent region on its undamaged homolog and use that sequence to rebuild the missing material.

The researchers have named this mechanism break-induced homologous extension repair, or BIHER.

Where damage is sufficiently extensive, repair requires several rounds. In other words, successive generations of rotifers each contribute to resolving the damage. The especially remarkable aspect is that the results indicate a damaged chromosome may ultimately be restored in full.

"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."

Desiccation may explain Adineta vaga's radiation resistance

It is reasonable to ask why A. vaga would need such a powerful defence against ionising radiation in the first place.

The explanation lies in its mossy home.

Mosses and lichens may remain dry for extended periods before becoming wet again, forcing their tiny residents to evolve survival strategies for these extremes. Bdelloid rotifers – and tardigrades too – cope by entering a state of near-total desiccation, essentially drying out as though it were an extreme sport.

Yet desiccation is exceptionally damaging to DNA. It can produce the same forms of physical damage caused by ionising radiation, including double-strand breaks capable of shattering chromosomes.

Consequently, A. vaga probably did not develop its remarkable repair capacity in response to radiation itself. Its radiation resistance seems instead to be an accidental benefit of adapting to repeated cycles 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."

Its capacity to survive while its genome is in complete disarray could also make A. vaga valuable for studying other circumstances in which chromosomes sustain catastrophic damage.

For instance, human explorers on Mars are likely to encounter radiation doses regarded as dangerous for people. Cancer cells, meanwhile, can undergo a process called chromothripsis, where chromosomes shatter and are rejoined in drastically rearranged configurations.

"Sometimes I say rotifer is like a living cancer, so it's a very interesting model system for all this research," Van Doninck said.

Questions still remain. The team now hopes to understand more clearly the molecular machinery that enables A. vaga to carry out such remarkable repairs, as well as whether comparable strategies exist elsewhere in nature.

Van Doninck added that the researchers are also examining what happens if both homologous chromosomes break at the same point. In that situation, the rotifer lacks the intact template on which BIHER usually depends – and we are equally eager to know the answer.

This is a microscopic creature that is probably living in your garden, yet it possesses an astonishing self-repair ability that may reveal something about surviving under the harshest conditions. That is 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 were 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.