Abstract
BackgroundHibernation is a physiological state exploited by many animals exposed to prolonged adverse environmental conditions associated with winter. Large changes in metabolism and cellular function occur, with many stress response pathways modulated to tolerate physiological challenges that might otherwise be lethal. Many studies have sought to elucidate the molecular mechanisms of mammalian hibernation, but detailed analyses are lacking in reptiles. Here we examine gene expression in the Australian central bearded dragon (Pogona vitticeps) using mRNA-seq and label-free quantitative mass spectrometry in matched brain, heart and skeletal muscle samples from animals at late hibernation, 2 days post-arousal and 2 months post-arousal.ResultsWe identified differentially expressed genes in all tissues between hibernation and post-arousal time points; with 4264 differentially expressed genes in brain, 5340 differentially expressed genes in heart, and 5587 differentially expressed genes in skeletal muscle. Furthermore, we identified 2482 differentially expressed genes across all tissues. Proteomic analysis identified 743 proteins (58 differentially expressed) in brain, 535 (57 differentially expressed) in heart, and 337 (36 differentially expressed) in skeletal muscle. Tissue-specific analyses revealed enrichment of protective mechanisms in all tissues, including neuroprotective pathways in brain, cardiac hypertrophic processes in heart, and atrophy protective pathways in skeletal muscle. In all tissues stress response pathways were induced during hibernation, as well as evidence for gene expression regulation at transcription, translation and post-translation.ConclusionsThese results reveal critical stress response pathways and protective mechanisms that allow for maintenance of both tissue-specific function, and survival during hibernation in the central bearded dragon. Furthermore, we provide evidence for multiple levels of gene expression regulation during hibernation, particularly enrichment of miRNA-mediated translational repression machinery; a process that would allow for rapid and energy efficient reactivation of translation from mature mRNA molecules at arousal. This study is the first molecular investigation of its kind in a hibernating reptile, and identifies strategies not yet observed in other hibernators to cope stress associated with this remarkable state of metabolic depression.
Highlights
Hibernation is a physiological state exploited by many animals exposed to prolonged adverse environmental conditions associated with winter
We discovered tissue-specific pathways that protect against the stress of reptilian hibernation and provide the evidence for multiple levels of gene expression regulation that may govern the physiological changes associated with hibernation
Each tile in the heatmap shows the normalized expression of a gene (Z-score), which was calculated by subtracting the mean expression value of a gene across all samples from the sample specific expression value, divided by the standard deviation of the mean expression value of the gene
Summary
Hibernation is a physiological state exploited by many animals exposed to prolonged adverse environmental conditions associated with winter. Many studies have sought to elucidate the molecular mechanisms of mammalian hibernation, but detailed analyses are lacking in reptiles. Hibernation is an extreme state of inactivity used among diverse animal lineages to cope with low or unpredictable food availability and unfavourable seasonal conditions during winter. Hibernation involves long periods of hypometabolism (torpor), often interrupted by shorter periods of euthermia (interbout arousal). These periods of euthermia allow animals to rewarm and replenish gene and protein products; processes that are virtually halted during torpor [1]. Reptilian hibernation involves radical changes in behaviour and physiology [12]
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