The role of host traits and geography in shaping the gut microbiome of insectivorous bats

Abstract

The gut microbiome is a symbiotic microbial community associated with the host and plays multiple important roles in host physiology, nutrition, and health. A number of factors have been shown to influence the gut microbiome, among which diet is considered to be one of the most important; however, the relationship between diet composition and gut microbiota in wild mammals is still not well recognized. Herein, we characterized the gut microbiota of bats and examined the effects of diet, host taxa, body size, gender, elevation, and latitude on the gut microbiota. The cytochrome C oxidase subunit I (COI) gene and 16S rRNA gene amplicons were sequenced from the feces of eight insectivorous bat species in southern China, including Miniopterus fuliginosus, Aselliscus stoliczkanus, Myotis laniger, Rhinolophus episcopus, Rhinolophus osgoodi, Rhinolophus ferrumequinum, Rhinolophus affinis, and Rhinolophus pusillus. The results showed that the composition of gut microbiome and diet exhibited significant differences among bat species. Diet composition and gut microbiota were significantly correlated at the order, family, genus, and operational taxonomic unit levels, while certain insects had a marked effect on the gut microbiome at specific taxonomic levels. In addition, elevation, latitude, body weight of bats, and host species had significant effects on the gut microbiome, but phylosymbiosis between host phylogeny and gut microbiome was lacking. These findings clarify the relationship between gut microbiome and diet and contribute to improving our understanding of host ecology and the evolution of the gut microbiome in wild mammals.

Importance: The gut microbiome is critical for the adaptation of wildlife to the dynamic environment. Bats are the second-largest group of mammals with short intestinal tract, yet their gut microbiome is still poorly studied. Herein, we explored the relationships between gut microbiome and food composition, host taxa, body size, gender, elevation, and latitude. We found a significant association between diet composition and gut microbiome in insectivorous bats, with certain insect species having major impacts on gut microbiome. Factors like species taxa, body weight, elevation, and latitude also affected the gut microbiome, but we failed to detect phylosymbiosis between the host phylogeny and the gut microbiome. Overall, our study presents novel insights into how multiple factors shape the bat's gut microbiome together and provides a study case on host-microbe interactions in wildlife.

Keywords: 16S rRNA; diet composition; gut microbiome; high-throughput sequencing; insectivorous bats.

Fig 1

Plots showing the composition of the gut microbiome for each bat species at the (A) phylum and (B) genus levels. Nonmetric multidimensional scaling analysis of the beta diversity of the gut microbiomes among (C) samples per species, and (D) different geographic populations of R. episcopus. R. episcopus (HN), Hunan’s Rhinolophus episcopus; R. episcopus (JX), Jiangxi’s Rhinolophus episcopus; R. episcopus (YN), Yunnan’s Rhinolophus episcopus.

Fig 2

OTU overlap plots of gut microbiomes between bat species. (A) The UpSet plot of OTU overlap between all bat species; the upper bar indicates the number of overlapping OTUs, points crossed by a connecting line at the bottom indicate the overlapping species and the species are indicated at the left; (B) Venn diagram of OTU overlap of three R. episcopus populations.

Fig 3

Plots showing the composition of the diet for each bat species at the (A) phylum and (B) genus levels. Nonmetric multidimensional scaling analysis of the beta diversity of the composition of diet among (C) samples per species, and (D) different geographic populations of R. episcopus.

Fig 4

Correlation of the gut microbiome data set with the dietary data set at the genus level.

Fig 5

The heatmap of the 40 OTUs with the highest abundance in the gut microbiomes of eight insectivorous bats.

Fig 6

Map of sampling site distribution and elevation, with pie charts showing samples per species composition and proportions within habitats.