How to resist dry soil: transcriptional changes in a Mediterranean earthworm during aestivation

Abstract

Earthworms have a central role in ministering the terrestrial ecosystems. Aestivation is a form of dormancy employed by the organisms living in deserts and arid environments, when confronted with prolonged periods of drought. As a survival tactic, aestivation has been studied in sea cucumbers, land snails and frogs, however little is known about aestivating earthworms. To understand the global metabolic adjustments required for withstanding the harsh conditions of the ever more severe Iberian drought, we performed a global transcriptomic exploration of the endogeic earthworm Carpetania matritensis during aestivation. There were a total of 6,352 differentially expressed transcripts in the aestivating group, with 65% being downregulated. Based on GO and KEGG enrichment analyses, downregulated genes seem to indicate an overall metabolic depression during aestivation. We noted a reduction of protein turnover and macromolecule metabolism coupled with suppression of digestion. Upregulated genes, namely antioxidant genes and DNA repair genes showed signs of abiotic stress caused by ROS generation. Abiotic stress led to transcriptomic changes of genes involved in immune response, mostly affecting the NF-κB signalling pathway and changes in apoptotic genes, indicating the necessity of investigating these processes in a tissue specific manner. Lastly we uncovered a possible mechanism for water retention by nitrogenous waste accumulation. This study provides the first ever transcriptomic investigation done on earthworms in condition of prolonged drought and as such serves as a general framework for investigation on other earthworm species and other soil invertebrates, which is becoming increasingly important with the current scenario of climate change.