Deciphering functional redundancy in the human microbiome

Liang Tian, Xu-Wen Wang, Ang-Kun Wu, Yuhang Fan, Jonathan Friedman, Amber Dahlin, Matthew K. Waldor, George M. Weinstock, Scott T. Weiss and Yang-Yu Liu ()
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Liang Tian: Brigham and Women’s Hospital and Harvard Medical School
Xu-Wen Wang: Brigham and Women’s Hospital and Harvard Medical School
Ang-Kun Wu: Brigham and Women’s Hospital and Harvard Medical School
Yuhang Fan: Brigham and Women’s Hospital and Harvard Medical School
Jonathan Friedman: The Hebrew University of Jerusalem
Amber Dahlin: Brigham and Women’s Hospital and Harvard Medical School
Matthew K. Waldor: Brigham and Women’s Hospital and Harvard Medical School
George M. Weinstock: The Jackson Laboratory for Genomic Medicine
Scott T. Weiss: Brigham and Women’s Hospital and Harvard Medical School
Yang-Yu Liu: Brigham and Women’s Hospital and Harvard Medical School

Nature Communications, 2020, vol. 11, issue 1, 1-11

Abstract: Abstract Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved — implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stability and resilience of the human microbiome, but this hypothesis has never been quantitatively tested. The origin of functional redundancy is still 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 find that this network exhibits several topological features that favor high functional redundancy. Furthermore, we develop a simple genome evolution model to generate genomic content network, finding that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with key topological features that favor high functional redundancy. Finally, we analyze data from two published studies of fecal microbiota transplantation (FMT), finding that high functional redundancy of the recipient’s pre-FMT microbiota raises barriers to donor microbiota engraftment. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience.

Date: 2020
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DOI: 10.1038/s41467-020-19940-1

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