Allometry of animal-microbe interactions and global census of animal-associated microbes

Abstract

Animals live in close association with microorganisms, mostly prokaryotes, living in or on them as commensals, mutualists or parasites, and profoundly affecting host fitness. Most animal-microbe studies focus on microbial community structure; for this project, allometry (scaling of animal attributes with animal size) was applied to animal-microbe relationships across a range of species spanning 12 orders of magnitude in animal mass, from nematodes to whales. Microbial abundances per individual animal were gleaned from published literature and also microscopically counted in three species. Abundance of prokaryotes/individual versus animal mass scales as a nearly linear power function (exponent = 1.07, R(2) = 0.94). Combining this power function with allometry of animal abundance indicates that macrofauna have an outsized share of animal-associated microorganisms. The total number of animal-associated prokaryotes in Earth's land animals was calculated to be 1.3-1.4 × 10(25) cells and the total of marine animal-associated microbes was calculated to be 8.6-9.0 × 10(24) cells. Animal-associated microbes thus total 2.1-2.3 × 10(25) of the approximately 10(30) prokaryotes on the Earth. Microbes associated with humans comprise 3.3-3.5% of Earth's animal-associated microbes, and domestic animals harbour 14-20% of all animal-associated microbes, adding a new dimension to the scale of human impact on the biosphere. This novel allometric power function may reflect underlying mechanisms involving the transfer of energy and materials between microorganisms and their animal hosts. Microbial diversity indices of animal gut communities and gut microbial species richness for 60 mammals did not indicate significant scaling relationships with animal body mass; however, further research in this area is warranted.

Keywords: allometry; animals; microbiota; prokaryotes; symbiosis.

Figure 1.

Microbial counts of microorganisms per individual animal versus individual animal body mass (M, wet weight in gram), log–log plot.

Figure 2.

Diversity indices versus individual animal body mass (M, wet weight in grams), log–log plots. (a) Shannon–Wiener index; (b) evenness; (c) Simpson's index and (d) Chao 1 index.

Figure 3.

Total animal-associated microbial operational units (OTUs) as reported by Ley et al. [14], electronic supplementary material, for 60 species of mammals versus animal mass in gram wet weight, log–log plot.