Intra- and Interindividual Variations Mask Interspecies Variation in the Microbiota of Sympatric Peromyscus Populations

Abstract

bUsing populations of two sympatric Peromyscus species, we characterized the importance of the host species, physiology, environment, diet, and other factors in shaping the structure and dynamics of their gut microbiota. We performed a capture-markrelease experiment in which we obtained 16S rRNA gene sequence data from 49 animals at multiple time points. In addition, we performed 18S rRNA gene sequencing of the same samples to characterize the diet of each individual. Our analysis could not distinguish between the two species of Peromyscus on the basis of the structures of their microbiotas. However, we did observe a set of bacterial populations that were found in every animal. Most notable were abundant representatives of the genera Lactobacillus and Helicobacter. When we combined the 16S and 18S rRNA gene sequence analyses, we were unable to distinguish the communities on the basis of the animal's diet. Furthermore, there were no discernible differences in the structure of the gut communities based on the capture site or their developmental or physiological status. Finally, in contrast to humans, where each individual has a unique microbiota when sampled over years, among the animals captured in this study, the uniqueness of each microbiota was lost within a week of the original sampling. Wild populations provide an opportunity to study host-microbiota interactions as they originally evolved, and the ability to perform natural experiments will facilitate a greater understanding of the factors that shape the structure and function of the gut microbiota.T he mechanisms that give rise to differences in the structure of communities associated with hosts are poorly understood. Among humans, it is widely accepted that the bacterial species composition within the intestines (i.e., the gut microbiota) is unique to each person and that the composition of the microbiota is the product of various factors, including the individual's genetics, diet, immune system, and behaviors (1). The amount that each of these contributes to shaping of the microbiota is unclear. Regardless, it is apparent that individuals within a family tend to harbor a more similar microbiota than others, leading to the suggestion that a person's microbiota is obtained horizontally as it is seeded by those in the environment (e.g., parents and siblings) and shaped via selection by a common culture, environment, and diet (2-5). This process of host selection and transmission has led to the hypothesis that the structure of the human gut microbiota and animal-associated communities, in general, is the result of coevolutionary processes (6).Given that evolutionary divergence among hosts results in differences in physiology, diet, immunity, and behavior, it is reasonable to expect host-specific signatures within their microbiota. One approach has been the reciprocal transplants of gut contents between germfree animals (e.g., zebrafish to mice, mice to zebrafish) in which the altered niche space of the host environment results in a remodeling of the inoculat...

Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals

“…However, among closely related primate species, diet obscures the signal of host phylogeny in gut microbial composition. Epidemiological studies in wildlife have elucidated crossspecies transmission of pathogens [64,100], but little is known about the transfer of commensal microbes among co-occurring wild animal populations [28,97]. More comprehensive comparative studies of wild mammal microbiomes are needed to fully resolve the dynamic dietary, physiological, social, and environmental factors that constrain gut microbiome ecology and evolution.…”

“…Most of these comparative microbiome surveys have sampled geographically and ecologically distinct captive or wild populations (but see [14,27,28]). However, captivity alters microbiome composition in mammals [12,[29][30][31], and, when animals are compared across geographic regions, host phylogenetic differences may be confounded by differences in local microbial taxa [15,32].…”

Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico

“…Numerous studies performed on nonlaboratory animals have reported similar degrees of variation between individual microbiotas (De Filippo et al 2010, Osei-Poku et al 2012, Hird et al 2014, Baxter et al 2015, which likely refl ects the multitude of environmental and physiological factors which can infl uence microbial assemblages. In the current study a variety of factors which could not be controlled for likely infl uenced the observed inter-individual variation.…”

A method to distinguish morphologically similar Peromyscus species using extracellular RNA and high-resolution melt analysis

“…its genetic structure of highly conserved regions surrounding hypervariable regions thereby allowing the use of universal primers for the study of microbiota in intestinal samples [22,23] . Our primers were designed for highly conserved regions in the two known species, M. musculus and P. leucopus, that surround a region of variability, and were then used to amplify that same region and test whether that amplicon allows species identification between P. leucopus and P. maniculatus using HRM technology.…”