Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric peromyscus populations

Abstract

Using 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-mark-release 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.

FIG 1

Spatial sampling of P. leucopus (A) and P. m. gracilis (B) indicates that their habitats overlap.

FIG 2

The microbiotas of P. leucopus and P. m. gracilis could not be differentiated on the basis of 16S rRNA gene sequences. Open and closed circles represent the results for P. leucopus and P. m. gracilis, respectively. The alpha diversity of the two species was calculated on the basis of the number of observed OTUs, Shannon diversity, and phylogenetic diversity; the metrics did not differ significantly between the species of mice (A). The median θ_YC and weighted UniFrac distances among mice within the same species and across species were large, and the difference was not significant (B). The relative abundances of two OTUs were significantly different between the two species; however, the effect of the size and relative abundance of those OTUs was small (C).

FIG 3

A core microbiota exists across mice of both Peromyscus species. The relative abundance of the OTUs (A) and genera and other taxa (B) that were found in at least 90% of the mice. The limit of detection was 0.02%.

FIG 4

Effects of age (A) and weight (B) on richness and diversity.

FIG 5

The individualized structure of the Peromyscus microbiota is transient. The median intra-animal distances between samples were significantly lower than the median interanimal distances (A). To compare the change in distance with time (B), time windows were selected so that there were approximately the same number of distances between the same animals per window. The position along the x axis was determined by the mean number of days between samples for the distances within the window and was jittered so the points for the two comparisons did not overlap; the vertical bars on the x axis indicate the boundaries of each window. The squares represent the median distance, and the lengths of the error bars reflect the 95% confidence intervals, with short lines representing the interquartile range. The asterisk indicates that intraindividual distances were significantly smaller than interindividual differences during the first 3 days of sampling.