Abstract

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.

Highlights

  • The continuous co-evolution of mammals and their gut microbes forms a complex relationship that provides benefits for both partners (Ley et al, 2008a,b)

  • A total of 1,327,632 16S ribosomal RNA (rRNA) gene reads were obtained, from which 1,750 operational taxonomic units (OTUs) were identified to be from gut microbiotas of 39 bats

  • The alpha diversity value was highest in the late summer, followed by early spring and early winter, and lowest in the early summer (Figure 1 and Supplementary Figure 1)

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Summary

Introduction

The continuous co-evolution of mammals and their gut microbes forms a complex relationship that provides benefits for both partners (Ley et al, 2008a,b). The host provides sufficient nutrients and suitable living conditions for the microorganisms, and affects the structure and composition of microorganisms in many ways, including genetics, immune status, intestinal environment, and diet (Faith et al, 2011; David et al, 2014). Host diet provides the major source of substrates that support microbial growth, microbes can use host-derived substrates, including mucus glycans, nutrients in sloughed epithelial cells, and biliary secretions (Leser et al, 2000; Hooper et al, 2002; Sonnenburg et al, 2005). When the host is fasting, there are few or no dietary substrates available for intestinal microbes. Prolonging the fasting period of the host may result in the selective development of gut microbes toward microbial communities capable of decomposing host-derived substrates (e.g., mucin)

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