Host-Specific Evolutionary and Transmission Dynamics Shape the Functional Diversification of Staphylococcus epidermidis in Human Skin.

Document Type

Article

Publication Date

2-6-2020

Keywords

JGM, JAXCC

JAX Source

Cell 2020 Feb 6; 180(3):454-470.e18

Volume

180

Issue

3

First Page

454

Last Page

470

ISSN

1097-4172

PMID

32004459

DOI

https://doi.org/10.1016/j.cell.2020.01.006

Grant

Jackson Laboratory Scientific Services Innovation Fund, GM126893,NS105539,AI142733,AR075174,AR073562,Department of Defense,National Science Foundation, American Cancer Society and the LEO Foundation

Abstract

Metagenomic inferences of bacterial strain diversity and infectious disease transmission studies largely assume a dominant, within-individual haplotype. We hypothesize that within-individual bacterial population diversity is critical for homeostasis of a healthy microbiome and infection risk. We characterized the evolutionary trajectory and functional distribution of Staphylococcus epidermidis-a keystone skin microbe and opportunistic pathogen. Analyzing 1,482 S. epidermidis genomes from 5 healthy individuals, we found that skin S. epidermidis isolates coalesce into multiple founder lineages rather than a single colonizer. Transmission events, natural selection, and pervasive horizontal gene transfer result in population admixture within skin sites and dissemination of antibiotic resistance genes within-individual. We provide experimental evidence for how admixture can modulate virulence and metabolism. Leveraging data on the contextual microbiome, we assess how interspecies interactions can shape genetic diversity and mobile gene elements. Our study provides insights into how within-individual evolution of human skin microbes shapes their functional diversification.

Comments

We would like to thank the Microbial Genomic Services and Mark Adams of The Jackson Laboratory for their support in sequencing and Mark Adams and the Oh lab for critical reading of the manuscript.

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