Adaptive Evolution within Gut Microbiomes of Healthy People

Shijie Zhao; Tami D Lieberman; Mathilde Poyet; Kathryn M Kauffman; Sean M Gibbons; Mathieu Groussin; Ramnik J Xavier; Eric J Alm

doi:10.1016/j.chom.2019.03.007

Adaptive Evolution within Gut Microbiomes of Healthy People

Cell Host Microbe. 2019 May 8;25(5):656-667.e8. doi: 10.1016/j.chom.2019.03.007. Epub 2019 Apr 23.

Authors

Shijie Zhao¹, Tami D Lieberman², Mathilde Poyet³, Kathryn M Kauffman⁴, Sean M Gibbons⁵, Mathieu Groussin³, Ramnik J Xavier⁶, Eric J Alm⁷

Affiliations

¹ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA.
² Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA; Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA; Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. Electronic address: tami@mit.edu.
³ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁴ Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
⁵ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA; Institute for Systems Biology, Seattle, WA 98109, USA; eScience Institute, University of Washington, Seattle, WA 98195, USA.
⁶ Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA; Gastrointestinal Unit, Massachusetts General Hospital, Boston, MA, USA; Center for Computational and Integrative Biology, Massachusetts General Hospital, Boston, MA, USA.
⁷ Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, MA, USA; Broad Institute of MIT and Harvard, Cambridge, MA, USA; Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. Electronic address: ejalm@mit.edu.

Abstract

Natural selection shapes bacterial evolution in all environments. However, the extent to which commensal bacteria diversify and adapt within the human gut remains unclear. Here, we combine culture-based population genomics and metagenomics to investigate the within-microbiome evolution of Bacteroides fragilis. We find that intra-individual B. fragilis populations contain substantial de novo nucleotide and mobile element diversity, preserving years of within-person history. This history reveals multiple signatures of within-person adaptation, including parallel evolution in sixteen genes. Many of these genes are implicated in cell-envelope biosynthesis and polysaccharide utilization. Tracking evolutionary trajectories using near-daily metagenomic sampling, we find evidence for years-long coexistence in one subject despite adaptive dynamics. We used public metagenomes to investigate one adaptive mutation common in our cohort and found that it emerges frequently in Western, but not Chinese, microbiomes. Collectively, these results demonstrate that B. fragilis adapts within individual microbiomes, pointing to factors that promote long-term gut colonization.

Keywords: Bacteroides; adaptive evolution; de novo mutation; horizontal gene transfer; human microbiome; metagenomics; microbial evolution; microbial genomics; whole-genome sequencing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adaptation, Biological*
Adult
Bacteroides fragilis / genetics*
Bacteroides fragilis / growth & development*
Female
Gastrointestinal Microbiome*
Genetics, Population
Healthy Volunteers
Humans
Male
Metagenomics
Microbiota*
Mutation
Selection, Genetic
Young Adult

Grants and funding

P30 DK043351/DK/NIDDK NIH HHS/United States