Special Features of Bat Microbiota Differ From Those of Terrestrial Mammals

Abstract

Bats (order Chiroptera) are one of the most diverse and widely distributed group of mammals with a close relationship to humans. Over the past few decades, a number of studies have been performed on bat viruses; in contrast, bacterial pathogens carried by bats were largely neglected. As more bacterial pathogens are being identified from bats, the need to study their natural microbiota is becoming urgent. In the current study, fecal samples of four bat species from different locations of China were analyzed for their microbiota composition. Together with the results of others, we concluded that bat microbiota is most commonly dominated by Firmicutes and Proteobacteria; the strict anaerobic phylum Bacteroidetes, which is dominant in other terrestrial mammals, especially humans and mice, is relatively rare in bats. This phenomenon was interpreted as a result of a highly specified gastrointestinal tract in adaptation to the flying lifestyle of bats. Further comparative study implied that bat microbiota resemble those of the order Carnivora. To discover potential bacterial pathogens, a database was generated containing the 16S rRNA gene sequences of known bacterial pathogens. Potential bacterial pathogens belonging to 12 genera were detected such as Salmonella, Shigella, and Yersinia, among which some have been previously reported in bats. This study demonstrated high resolution and repeatability in detecting organisms of rare existence, and the results could be used as guidance for future bacterial pathogen isolation.

Keywords: aerobic microbes; bacterial pathogen; bat; gut microbiota; sequencing.

FIGURE 1

A map showing the four bat sample collection locations in China.

FIGURE 2

Phylogenetic dendrogram constructed from Cyto b gene sequences of bats. According to traditional classification, Eonycteris spelaea belong to the Megachiroptera suborder and the others belong to the Microchiroptera suborder.

FIGURE 3

Diversity of bacterial communities as revealed by a rarefaction curve constructed from OTUs at 3% (A) and 5% (B) dissimilarity levels.

FIGURE 4

Taxonomic classification of pyrosequencing reads at phylum level (A) and family level (B) using the RDP classifier at a confidence threshold of 70%.

FIGURE 5

Dendrogram showing the similarity of bacterial communities based on the (A) Yue and Clayton measure of dissimilarity and (B) Bray–Curtis index.

FIGURE 6

Principal coordinate analysis of UniFrac metric for all samples: (A) PC1 and PC2 and (B) PC1 and PC3.

FIGURE 7

Comparison of bat microbiota with that of other mammals (unweighted UniFrac analysis). Reference sequence data from Ley et al. (2008) were trimmed to match the same position and length of the 16S rRNA gene. Different colors represent different feeding habits (green: herbivorous, red: carnivorous, gray: omnivorous) except blue which marked our sample. Abbreviations of species: orangutans, Orang1,2; western lowland gorillas, GOR and GORSD; chimpanzees, CHIMP1,12; black rhinoceros, BNO; flying fox, FF; bighorn sheep, BHSD, BH1, and BH2; horses, HORSEJ and HORSEM; Somali wild ass, WA; Grevy’s zebra, GZ; Asian elephants, AE1-3; rock hyraxes, RH and RHSD; Capybara, CAP; Bwindi gorilla, BG; giraffe, gir; springboks, SBK; Okapi, OK1-3; Transcaspian Urial sheep, TU1,2; Speke’s gazelles, SP3; Argali sheep, AS1-3; takin, TAK; François langur, FL; springboks, SB and SBSD; douc langur, DL; eastern black and white colobus, COL; red kangaroos, KO1,2; red river hog, RRH; baboons, AFBAB; Indian rhinoceros, IR; naked mole rat, MOLERAT; Visayan warty pig, VWP; babirusa, BARB; spotted hyenas, HY1,2; East Angolan colobus, EAC; ring-tailed lemur, RT; white-faced saki, Saki; Prevost’s squirrel, SQ; spider monkey, SPIM; mongoose lemur, ML; black lemur, BKLE; calimicos (Goeldi’s marmoset), CAL; Geoffrey’s marmoset, MAR; bush dogs, bdog1,3; armadillo, arma; lions, Li1-3; cheetahs, CE2,3; African elephants, AFEL, AFYEL, AFEL2,3; Hartmann’s mountain zebra, AFZEB; red panda, RP and RPSD; polar bears, PB1,2; hedgehog, HH; spectacled bear, SB; giant panda, GP; black bears, BB1,2; Seba’s short-tailed bat, bat; echidna, ECH; rabbit, RA.

FIGURE 8

Heatmap of detected potential bacterial pathogens. The strains in brackets represent the pathogenic bacteria used for retrieval and comparison.