Abstract
The gut microbiome is a community of host-associated symbiotic microbes that fulfills multiple key roles in host metabolism, immune function, and tissue development. Given the ability of the microbiome to impact host fitness, there is increasing interest in studying the microbiome of wild animals to better understand these communities in the context of host ecology and evolution. Human microbiome research protocols are well established, but wildlife microbiome research is still a developing field. Currently, there is no standardized set of best practices guiding the collection of microbiome samples from wildlife. Gut microflora are typically sampled either by fecal collection, rectal swabbing, or by destructively sampling the intestinal contents of the host animal. Studies rarely include more than one sampling technique and no comparison of these methods currently exists for a wild mammal. Although some studies have hypothesized that the fecal microbiome is a nested subset of the intestinal microbiome, this hypothesis has not been formally tested. To address these issues, we examined guano (feces) and distal intestinal mucosa from 19 species of free-ranging bats from Lamanai, Belize, using 16S rRNA amplicon sequencing to compare microbial communities across sample types. We found that the diversity and composition of intestine and guano samples differed substantially. In addition, we conclude that signatures of host evolution are retained by studying gut microbiomes based on mucosal tissue samples, but not fecal samples. Conversely, fecal samples retained more signal of host diet than intestinal samples. These results suggest that fecal and intestinal sampling methods are not interchangeable, and that these two microbiotas record different information about the host from which they are isolated.
Highlights
The vertebrate bacterial gut microbiome is intimately linked to host physiology, nutrition, and health (e.g., Hooper et al, 2012; Sommer and Bäckhed, 2013; The Human Microbiome Project Consortium, 2013; Mosca et al, 2016)
All research was conducted in accordance with accepted standards for humane capture, handling, and sacrifice of bats published by the American Society of Mammalogists (Sikes et al, 2016) and approved Institutional Animal Care and Use Committee protocols (AMNH IACUC 20170403)
While insectivorous bat species seem to have high microbial diversity (Figure 1). These results are consistent with a previous study, which found insectivorous bat species to have the most diverse microbiomes; within the phyllostomids, the same study found D. rotundus to have the most depauperate microbiome, with insect eating and plant visiting species to be slightly more diverse (Phillips et al, 2012)
Summary
The vertebrate bacterial gut microbiome is intimately linked to host physiology, nutrition, and health (e.g., Hooper et al, 2012; Sommer and Bäckhed, 2013; The Human Microbiome Project Consortium, 2013; Mosca et al, 2016). The advent of culturefree metagenomic techniques has created a microbial ecology revolution wherein researchers can assess the composition, diversity, and structure of microbes in relation to their host animals (Gilbert et al, 2014). While most microbiome research has focused on humans and model organisms, microbiome studies in wildlife have recently gained popularity in light of the potential power of the microbiome to shape host evolution and ecology (e.g., Ley et al, 2008; Amato, 2013; Hird, 2017). In order to draw biologically meaningful inferences across such studies, it is essential to develop protocols that minimize bias and artifacts in samples collected from wild organisms. No study currently addresses whether different collection methods have similar impacts on downstream microbial community analyses in wild mammals
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