Dataset Information

Gut transcriptomic changes during hibernation in the greater horseshoe bat (Rhinolophus ferrumequinum).

ABSTRACT:

Background

The gut is the major organ for nutrient absorption and immune response in the body of animals. Although effects of fasting on the gut functions have been extensively studied in model animals (e.g. mice), little is known about the response of the gut to fasting in a natural condition (e.g. hibernation). During hibernation, animals endure the long term of fasting and hypothermia.

Results

Here we generated the first gut transcriptome in a wild hibernating bat (Rhinolophus ferrumequinum). We identified 1614 differentially expressed genes (DEGs) during four physiological states (Torpor, Arousal, Winter Active and Summer Active). Gene co-expression network analysis assigns 926 DEGs into six modules associated with Torpor and Arousal. Our results reveal that in response to the stress of luminal nutrient deficiency during hibernation, the gut helps to reduce food intake by overexpressing genes (e.g. CCK and GPR17) that regulate the sensitivity to insulin and leptin. At the same time, the gut contributes energy supply by overexpressing genes that increase capacity for ketogenesis (HMGCS2) and selective autophagy (TEX264). Furthermore, we identified separate sets of multiple DEGs upregulated in Torpor and Arousal whose functions are involved in innate immunity.

Conclusion

This is the first gut transcriptome of a hibernating mammal. Our study identified candidate genes associated with regulation of food intake and enhance of innate immunity in the gut during hibernation. By comparing with previous studies, we found that two DEGs (CPE and HSPA8) were also significantly elevated during torpor in liver and brain of R. ferrumequinum and several DEGs (e.g. TXNIP and PDK1/4) were commonly upregulated during torpor in multiple tissues of different mammals. Our results support that shared expression changes may underlie the hibernation phenotype by most mammals.

SUBMITTER: Sun H

PROVIDER: S-EPMC7366455 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:A large number of microorganisms colonize the intestines of animals. The gut microbiota plays an important role in nutrient metabolism and affects a number of physiological mechanisms in the host. Studies have shown that seasonal changes occur in the intestinal microbes of mammals that hibernate seasonally. However, these studies only focused on ground squirrels and bears. It remains unclear how hibernation might affect the intestinal microbes of bats. In this study, we measured microbial diversity and composition in the gut of Rhinolophus ferrumequinum in different periods (early spring, early summer, late summer, torpor, and interbout arousal) using 16S ribosomal RNA gene amplicon sequencing and PICRUSt to predict functional profiles. We found seasonal changes in the diversity and composition of the gut microbes in R. ferrumequinum. The diversity of gut microbiota was highest in the late summer and lowest in the early summer. The relative abundance of Proteobacteria was highest in the early summer and significantly lower in other periods. The relative abundance of Firmicutes was lowest in the early summer and significantly increased in the late summer, followed by a significant decrease in the early winter and early spring. The relative abundance of Tenericutes was significantly higher in the early spring compared with other periods. The results of functional prediction by PICRUSt showed seasonal variations in the relative abundance of metabolism-related pathways, including lipid metabolism, carbohydrate metabolism, and energy metabolism. Functional categories for carbohydrate metabolism had significantly lower relative abundance in early winter-torpor compared with late summer, while those associated with lipid metabolism had significantly higher relative abundance in the early winter compared with late summer. Overall, our results show that seasonal physiological changes associated with hibernation alter the gut microbial community of R. ferrumequinum. Hibernation may also alter the metabolic function of intestinal microbes, possibly by converting the gut microflora from carbohydrate-related to lipid-related functional categories. This study deepens our understanding of the symbiosis between hibernating mammals and gut microbes.