Interspecific and intraspecific Taylor's laws for frog skin microbes

Abstract

Amphibians are known to have an abundance of microorganisms colonizing their skin, and these symbionts often protect the host from disease. There are now many comprehensive studies on amphibian skin microbes, but the interspecific and intraspecific abundance distributions (or abundance heterogeneity) of amphibian skin microbes remain unclear. Furthermore, we have a very limited understanding of how the abundance and heterogeneity of microbial communities relate to the body size (or more specifically, skin surface area) of amphibian hosts. In this study, we evaluated the interspecific and intraspecific abundance distribution patterns of amphibian skin microbes and evaluated whether the symbiotic skin microbes of different anuran species share a fundamental heterogeneity scaling parameter. If scaling invariance exists, we hypothesize that a fundamental heterogeneity scaling value also exists. A total of 358 specimens of 10 amphibian host species were collected, and we used Type-I and III Taylor's power law expansions (TPLE) to assess amphibian skin microbial heterogeneity at the community and mixed-species population levels, respectively. The obtained results showed that, at the community scale, a high aggregation of the microbial abundance distribution on the skin barely changed with host size. In a mixed-species population (i.e., a community context), the abundance distribution pattern of mixed microbial species populations also does not change with host size and always remains highly aggregated. These findings suggest that while amphibian skin microbiomes located in different hosts may have different environmental conditions, they share a fundamental heterogeneity scaling parameter, and thus, scale invariance exists. Finally, we found that microhabitat area provided by the host skin is vital to the stability of the symbiotic microbial community.

Keywords: Anura microbiota; Symbiotic microbial community; Taylor’s Power Law Extensions.

Graphical abstract

Fig. 1

Relative abundance of microbes at the phylum classification level (the top 13 most abundant bacterial phyla) among skin bacterial communities of all amphibian host species studied.

Fig. 2

Alpha diversity of different amphibian skin microbial communities. Note that significant differences in the Shannon values were always found between all pairs of different host species (Kruskal-Wallis tests, p < 0.001).

Fig. 3

Analysis of similarity (ANOSIM) of the microbial community composition between hosts based on Bray–Curtis distance.

Fig. 4

Graph of fitting Type-I PLE (left) and Type-III PLE (right) with all 358 samples of the amphibian skin microbiome. The slope (b1) of the Type-I PLE measures the community spatial heterogeneity; the slope (b3) of the Type-III PLE measures the spatial heterogeneity of mixed species.

Fig. 5

Scatter diagram of the mean variance relationship of symbiotic microbial communities of different host species based on the Type-I model.

Fig. 6

Scatter diagram of the mean variance relationship of symbiotic microbial communities of different host species based on the type III model.

Fig. 7

Relationship between the three-dimensional skin area of different host species and parameter b calculated by the corresponding Type-I and Type-III models.