Have you ever left your house on a sweltering day and immediately gone back inside because it is too hot to even think? Not all creatures have the luxury of escaping torrid heat, so some have found ways to survive even when their homes become as dry as a bone. They can either deal with water shortages and scorching temperatures or use a hibernation-like ‘summer sleep’ called aestivation, when they become inactive and shut off most biological processes except those necessary for survival. Aestivating animals such as earthworms can alter which genes they turn off and on to survive until the rains return. These stoic burrowers are also true unsung heroes in our battle against the effects of climate change because they help store carbon in the ground and help other smaller animals by providing shelter while they undergo aestivation. Since scientists predict climate change will increase the number of droughts, figuring out how these climate change mitigators aestivate during an exceptionally dry summer is critical. Natasha Tilikj and Marta Novo from the Complutense University of Madrid, Spain, investigated which genes earthworms (Carpetania matritensis) from the Iberian Peninsula activate and switch off during aestivation.

The duo collected earthworms from El Molar, Spain, and returned with them to the lab. Once there, the team needed the right soil conditions to produce both active and aestivating worms – when they tie themselves into mucus-covered knots – to compare the two. To reproduce the correct conditions, they placed some worms in dry soil to encourage them to begin aestivating and maintained the remaining worms in moist soil to keep them active. After a month, the team checked whether or not the worms were aestivating and then analyzed how the animals changed the patterns of gene expression – which genes they upregulated and which they downregulated – after slipping into a summer sleep.

Unsurprisingly, the team found that the aestivating worms reduced expression of most genes. Other aestivating animals conserve energy by destroying and producing fewer proteins, to extend their state of suspended animation until conditions improve, and worms could be using the same strategy. The aestivating worms reduced expression of genes involved in the production of proteins and other macromolecules in addition to genes involved in protein breakdown and digestion. As worms go into this state of dormancy, they shut down processes that are not vital for survival. The team also found evidence that the worms were under stress and increased the levels of toxic oxygen by-products, known as reactive oxygen species, which can damage DNA after aestivation. In addition, there was an increase in the expression of genes that typically help combat and repair the DNA damage caused by these harmful products, and the stress experienced by the worms also activated the worms’ immune response for protection from possible infection.

Finally, the team discovered that aestivating worms may stave off water loss using an innovative mechanism that researchers have yet to study in earthworms: the worms increased the expression of genes involved in the production of the amino acid arginine. The duo suggest that an increase in arginine, or a build-up of nitrogenous waste, might reduce the amount of water lost by the worms.

Aestivating earthworms employ various strategies to survive desiccation. With increasing drought in the future, whether these protective mechanisms will be sufficient is unknown. The researchers recommend further investigation into the role of digestion, excretion and the central nervous system in aestivation to help scientists design better drought mitigation strategies to protect these uncelebrated champions of the subterranean world.

How to resist soil desiccation: Transcriptional changes in a Mediterranean earthworm during aestivation
Comp. Biochem. Physiol. A.
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