Adaptive Evolution within Gut Microbiomes of Healthy People

• Published in: Cell host & microbe Vol. 25; no. 5; pp. 656 - 667.e8
• Main Authors: Zhao, Shijie, Lieberman, Tami D., Poyet, Mathilde, Kauffman, Kathryn M., Gibbons, Sean M., Groussin, Mathieu, Xavier, Ramnik J., Alm, Eric J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 08.05.2019
• Subjects: Adaptation, Biological; adaptive evolution; Adult; Bacteroides; Bacteroides fragilis - genetics; Bacteroides fragilis - growth & development; de novo mutation; Female; Gastrointestinal Microbiome; Genetics, Population; Healthy Volunteers; horizontal gene transfer; human microbiome; Humans; Male; Metagenomics; microbial evolution; microbial genomics; Microbiota; Mutation; Selection, Genetic; whole-genome sequencing; Young Adult; de novo mutation; human microbiome; metagenomics; whole-genome sequencing; microbial evolution; adaptive evolution; horizontal gene transfer; microbial genomics; Bacteroides
• ISSN: 1931-3128; 1934-6069; 1934-6069
• DOI: 10.1016/j.chom.2019.03.007

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. [Display omitted] •Bacteroides fragilis adapts via de novo mutations within healthy people•Polysaccharide utilization and capsule synthesis pathways change during colonization•B. fragilis diversifies into coexisting sublineages within individuals•An adaptive mutation emerges with different likelihood between human populations Bacteria acquire adaptive mutations during infections, but the role of mutations in the gut microbiome is unknown. Zhao and Lieberman et al. report that Bacteroides fragilis adapts via mutation within healthy people. They discover genes important to survival in humans and detail dynamics within individuals and across populations.