Cross-Scale Analyses of Animal and Human Gut Microbiome Assemblies from Metacommunity to Global Landscape

ABSTRACT

Animal (human) gut microbiomes have been coevolving with their hosts for many millions of years. Understanding how the coevolution shapes the processes of microbiome assembly and diversity maintenance is important but rather challenging. An effort may start with the understanding of how and why animals and humans may differ in their microbiome neutrality (stochasticity) levels. Here, we attempted to perform layered comparative stochasticity analyses across animal species (including humans), class, and kingdom scales, corresponding to microbial metacommunity, landscape, and global-landscape scales. By analyzing 4,903 microbiome samples from 274 animal species covering 4 major invertebrate classes and all 6 vertebrate classes and including 1,787 human gut microbiome samples, we discovered the following: (i) at the microbial metacommunity (animal species) scale, although the general trend of stochasticity (measured in the relationships between fundamental biodiversity/dispersal numbers of Hubbell’s neutral theory and host species phylogenetic timeline) seems continuous, there seems to be a turning point from animals to humans in the passing rate of neutrality tests (12% to 45% versus 100%). We postulate that it should be the human experiences from agricultural/industrial activities (e.g., diet effects) and frequent social/familial contacts that are responsible for the dramatically rising stochastic neutrality in human gut microbiomes. (ii) At the microbial landscape (animal class) and global landscape (animal kingdom) scales, neutrality is not detectable, suggesting that the landscape is niche differentiated—animal species may possess “home niches” for their coadapted microbiomes. We further analyze the reliabilities of our findings by using variable P value thresholds (type I error) and performing power analysis (type II error) of neutrality tests.

IMPORTANCE Understanding how the coevolution (evolutionary time scale) and/or the interactions (ecological time scale) between animal (human) gut microbiomes and their hosts shape the processes of the microbiome assembly and diversity maintenance is important but rather challenging. An effort may start with the understanding of how and why animals and humans may differ in their microbiome neutrality (stochasticity) levels. Here, we attempted to perform layered comparative stochasticity analyses across animal species (including humans), class, and kingdom scales, corresponding to microbial metacommunity, landscape, and global-landscape scales by analyzing 4,903 microbiome samples from 274 animal species covering 4 major invertebrate classes and all 6 vertebrate classes, and including 1,787 human gut microbiome samples. The analyses were implemented by fitting the multisite neutral model and further augmented by checking false-positive and false-negative errors, respectively. It appears that there is a turning (tipping) point in the neutrality level from animal to human microbiomes.