Comparison of Brain Transcriptome of the Greater Horseshoe Bats (Rhinolophus ferrumequinum) in Active and Torpid Episodes

Abstract

Hibernation is an energy-saving strategy which is widely adopted by heterothermic mammals to survive in the harsh environment. The greater horseshoe bat (Rhinolophus ferrumequinum) can hibernate for a long period in the hibernation season. However, the global gene expression changes between hibernation and non-hibernation season in the greater horseshoe bat remain largely unknown. We herein reported a comprehensive survey of differential gene expression in the brain between winter hibernating and summer active greater horseshoe bats using next-generation sequencing technology. A total of 90,314,174 reads were generated and we identified 1,573 differentially expressed genes between active and torpid states. Interestingly, we found that differentially expressed genes are over-represented in some GO categories (such as metabolic suppression, cellular stress responses and oxidative stress), which suggests neuroprotective strategies might play an important role in hibernation control mechanisms. Our results determined to what extent the brain tissue of the greater horseshoe bats differ in gene expression between summer active and winter hibernating states and provided comprehensive insights into the adaptive mechanisms of bat hibernation.

Gene expression and adaptive evolution of ZBED1 in the hibernating great horseshoe bat (Rhinolophus ferrumequinum)

“…This could suggest the existence of underlying mechanisms that allow hibernators to withstand these physiological extremes. To date, several possible protective mechanisms have been proposed (Carey et al, 2000;Cerri et al, 2009;Lei et al, 2014) and among them, increased cell proliferation appears to represent a major protective mechanism to compensate for increased apoptotic cells during hibernation (Cerri et al, 2009).…”

“…In order to survive, hibernators must suffer potential adverse effects induced by long periods of low body temperature, and repeated ischemia and perfusion, some of which are highly stressful and even lethal for non-hibernators (Carey et al, 2003). However, hibernators obviously have abilities to protect themselves from potential harm, and several underlying mechanisms are proposed, such as induced expression of stress (heat shock) proteins to combat cellular stress (Carey et al, 1999(Carey et al, , 2000Lei et al, 2014) and increased protein-ubiquitin conjugate concentration to help degrade damaged proteins during hibernation (Carey et al, 2000).…”

Mechanisms of oxidative stress resistance in the brain: Lessons learned from hypoxia tolerant extremophilic vertebrates

“…Studies from the hibernating greater horseshoe bat, Rhinolophus ferrumequinum , have demonstrated pronounced global gene differential expression in the brains between hibernating and non-hibernating seasons [90]. Specifically, glutathione peroxidase-3 gene activity (Table 1), which functions in H 2 O 2 detoxification, is increased by 8 fold in the active brain compared to the torpid brain for this horseshoe bat [90].…”

“…Studies from the hibernating greater horseshoe bat, Rhinolophus ferrumequinum , have demonstrated pronounced global gene differential expression in the brains between hibernating and non-hibernating seasons [90]. Specifically, glutathione peroxidase-3 gene activity (Table 1), which functions in H 2 O 2 detoxification, is increased by 8 fold in the active brain compared to the torpid brain for this horseshoe bat [90]. Trying to elucidate the mechanism by which hibernating squirrels are able to maintain low levels of oxidative stress throughout hibernation and arousal, it was reported that antioxidants rose in the ground squirrel ( Citellus citellus ) in response to winter conditions [91].…”

Blood miRNomes and transcriptomes reveal novel longevity mechanisms in the long-lived bat, Myotis myotis

“…Intriguingly, positive selection was also detected in mitochondrial-encoded and nuclear-encoded oxidative phosphorylation genes in bats, which may explain their efficient energy metabolism necessary for flight [15]. Apart from comparative genome analysis, only a small number of transcriptomic studies on bats using mRNA-Seq and miRNA-Seq technologies have been carried out, focused primarily on the characteristics of hibernation [16], immunity [17, 18], echolocation [19] and phylogeny [20]. However, the molecular mechanisms of adaptations affecting longevity are still far from understood, especially with respect to gene regulation.…”