Lineage-level within-species dynamics in the human facial skin microbiome

Abstract

Multiple lineages of a bacterial species can coexist in a community. These extremely closely-related clades originate from the recent immigration of individual cells, whose evolution over short timescales (years) results in minute genomic diversity (101 SNPs/genome). Each has distinct origins, and the mutations they contain can reveal their individual evolutionary and ecological history. However the difficulty of differentiating coexisting lineages limits the phylogenetic resolution at which community dynamics can be studied. Here, I describe methods to cluster large sets of diverse genomes into lineages and apply them to the observation of natural lineage-level assembly dynamics in the human facial skin microbiome. In Chapter 2, I use new methods to improve lineage-level clustering and delineate 4,055 genomes of C. acnes and S. epidermidis isolates from human facial skin into 167 lineages. In Chapter 3, I use these data to observe natural transmission events and assembly dynamics of the facial skin microbiome. I find that the gain and loss of individual C. acnes and S. epidermidis lineages underlies their apparent stability at the species level, and that these dynamics also change throughout the human lifespan. Lineages of S. epidermidis are replaced in unexpectedly fast cycles, and C. acnes lineages are acquired during developmentally-driven population expansion. By advancing current methods, I enabled the observation of new ecological dynamics at an unprecedented resolution. The dynamics described here will influence the development of therapeutic strains with durable engraftment, and inspire the study of their effects on hosts, such as the immune consequences of lineage-level turnover.