Highly-resolved within-species dynamics in the human facial skin microbiome

Abstract

Human facial skin microbiomes (FSMs) on adults are dominated by just two bacterial species,Cutibacterium acnesandStaphylococcus epidermidis.Underlying this apparent simplicity, each FSM harbors multiple strains of both species whose assembly dynamics on individuals are unknown. Here, we use 4,055 isolate genomes and 360 metagenomes to trace the dynamics of strains on individuals and their transmission. Strains are shared amongst family members of all ages, but each individual harbors unique strain consortia. Strain stability changes upon formation of the adult-type FSM:S. epidermidislineage turnover slows, and the rate ofC. acnescolonization increases before stabilizing, suggesting this transitional window could facilitate engraftment of therapeutic strains. Our work reveals previously undetectable community dynamics and informs the design of therapeutic interventions.One-Sentence SummaryPreviously undetectable gain and loss of individual strains underlies the species stability of important microbiome bacteria.

Intraspecies warfare restricts strain coexistence in human skin microbiomes

“…Published lineage assemblies 9 were annotated using Bakta and screened against specialist databases using AMRFinder 60 , VFDB 61 , Defense Finder 43 . Cluster of Orthologous Genes (COG terms) were assigned using eggnog-mapper v2 62 .…”

“…Intra-lineage single nucleotide variants (SNVs) phylogenies identified previously 9 were investigated for lineages 20 and 37, which had strong “all-or-nothing” intra-lineage variations in sensitivity (defined as >1000 ZOI AUC range). In addition, Breseq 65 was used to identify for putative insertion-deletion mutations in the same genes as identified SNVs in idiosyncratic isolates.…”

“…Phylogenetic trees were generated in Baker et al 9 . In that study, Widevariant 9 was used to tabulate core genome SNVs without signals of recombination.…”

“…Phylogenetic trees were generated in Baker et al 9 . In that study, Widevariant 9 was used to tabulate core genome SNVs without signals of recombination. RaXML v8.2.12 was used to construct a species-wide maximum parsimony tree from a representative isolate for each lineage and DNApars v3.5c was used to construct a lineage-wide maximum parsimony tree from all isolates of selected lineages.…”

“…To test if intraspecies warfare is a major barrier to S. epidermidis strain colonization, we examined antagonistic interactions among a collection of S. epidermidis isolates collected from extensively-sampled, nuclear family members 9 . Ecologically-relevant warfare should result in fewer antagonisms between strains on a person than expected by random assembly of available strains (Figure 1A).…”