Deciphering Functional Redundancy in the Human Microbiome

Abstract

Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved1-5---implying an ecological property known as functional redundancy. Such functional redundancy is thought to underlie the stability and resilience of the human microbiome6,7, but its origin is elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network --- a bipartite graph that links microbes to the genes in their genomes. We show that this network exhibits several topological features, such as highly nested structure and fat-tailed gene degree distribution, which favor high functional redundancy. To explain the origins of these topological features, we develop a simple genome evolution model that explicitly considers selection pressure, and the processes of gene gain and loss, and horizontal gene transfer. We find that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with both highly nested structure and fat-tailed gene degree distribution, and consequently favor high functional redundancy. These findings provide insights into the relationships between structure and function in complex microbial communities. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience.