Integrative omics approaches reveal mechanisms of combined heat stress and extreme hypoxia tolerance in a Cerambycid beetle larva

[Lien vers la fiche source] Atmospheric oxygen, which is essential for energy metabolism, can directly influence an animal's heat tolerance by affecting oxygen transport processes, especially in those living in oxygen-poor environments, such as inside plant tissues, underground or in aquatic environments. Yet, the interplay of oxygen and temperature are rarely studied together, limiting our ability to predict their combined effects on insect performance. This study examines the tolerance of a large xylophagous cerambycid beetle Cacosceles newmannii to combined hypoxic and thermal stress using performance assays (duration of righting response) coupled with transcriptomic and metabolomic analyses. Metabolomic profiling showed that most amino acids were downregulated in the body but upregulated in the haemolymph as stress increased. Transcriptomic profiles clustered primarily by temperature (25 °C vs 35 °C), independent of oxygen level. Consistently, both the number of differentially expressed genes and enriched GO terms were much higher between temperatures than between oxygen treatments. Cacosceles newmannii appears capable of modulating its performance to reduce the energy costs and physiological damage induced by hypoxia. This suggests a high baseline hypoxia tolerance rather than a rapid plastic (induced) physiological hypoxia response, probably due to the species' endophytic lifestyle. Conversely, thermal stress leads to a predictable increase in metabolic activity but does not markedly affect performance, triggering adjustments to maintain cellular functions while limiting the impact of stresses expected under conditions of high temperature, such as desiccation. In short, our study highlights the distinct metabolic pathways mobilised to cope with hypoxic versus thermal stress, emphasizing the importance of integrated approaches in understanding insect responses to environmental changes. These findings have significant implications for understanding the species' ecology, with applications for pest management and sustainable agriculture in the context of climate change. This dataset contains performance data acquired from Cacosceles newmannii. Performance was assessed under the different oxygen and temperature conditions both with and without an acclimation period of 6 days at the same conditions. It was estimated by measuring the time taken by larvae placed on their backs to turn over onto their ventral side. Larvae were subjected to all treatments in a random order, first without the acclimation period, and second after the 6-day acclimation period. Duration of righting was measured five times for each larva at each treatment. Larvae were given at least 5 days to recover between two treatments, and during a trial, larvae were allowed to rest for at least 5 minutes between each of the 5 replicate trials. Larvae were individually placed in a custom-made chamber built on a peltier heating surface and air was directed into the chamber at the desired oxygen level using an overpressure funnel system. Larvae were given 2 minutes before they were gently pushed onto their back with a thin wooden stick, in order to i) limit the effect of handling stress and ii) allow the oxygen level to equilibrate after the chamber was briefly open. The time needed for a larva to turn on its ventral side again was recorded to the second. Metabolomics data are published in the supplementary material of the associated article, and transcriptomics data have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB106986 ([https://www.ebi.ac.uk/ena/browser/view/PRJEB106986]) and will be available upon acceptance of the article.