Aging-related changes in the diversity of women's skin microbiomes associated with oral bacteria

Abstract

Skin aging is associated with changes in cutaneous physiology including interactions with a skin microbial community. A striking alteration and diversification in the skin microbiome with aging was observed between two different age groups of 37 healthy Japanese women, i.e. younger adults of 21-37 years old and older adults of 60-76 years old, using bacterial 16S rRNA gene sequencing. The analyses revealed that the alpha diversity/species richness was significantly higher in the older than the younger group for the cheek and forehead microbiomes, while the beta diversity in the overall structure significantly differed particularly for the forearm and scalp microbiomes between the two age groups. Taxonomic profiling showed a striking reduction in the relative abundance of the majority skin genus Propionibacterium in the cheek, forearm and forehead microbiomes of the older adults, and identified 38 species including many oral bacteria that significantly differentiated the two age groups with a skin site dependency. Furthermore, we found chronological age-related and unrelated skin clinical parameters that correlate with the observed changes in the skin microbiome diversity. Thus, our data suggested that the diversification of skin microbiomes in adult women was largely affected by chronological and physiological skin aging in association with oral bacteria.

Figure 1

Comparison of alpha diversity of four skin microbiomes between the younger and older groups. Differences in alpha diversity in each skin microbiome between the two age groups (n = 18, younger; n = 19, older group) are shown by three indices. Line in box is a median of index scores, boxes represent interquartile range, whiskers represent lowest and highest values, and dots represent outliers. Statistical significance is indicated by **p < 0.01 and *p < 0.05 (Welch’s t test).

Figure 2

UniFrac-PCoA of 37 skin microbiome samples. The weighted and unweighted UniFrac-PCoA for each skin microbiome is shown, respectively. Red and blue circles represent samples from older and younger subjects, respectively. R-values and p-values of ANOSIM between the two age groups in each skin location are shown below each graph.

Figure 3

Comparison of the relative abundance of major bacterial genera. The relative abundance of six major genera in the four skin microbiomes is compared between the younger and older groups. Statistically significant p-values are shown in blue.

Figure 4

Spatial distribution of the 38 species having significant changes in the abundance between the younger and older groups in the four skin sites. The results shown in Supplementary Table S4 are summarized in the Venn diagram.

Figure 5

Proportion of oral bacteria in the four skin microbiomes of the younger and older groups. Each dot indicates each subject’s sample. The y-axis indicates the number of reads assigned to the oral bacteria in a total of 2,500 reads per subject while the x-axis indicates subjects’ age. P-values are calculated by Mann-Whitney test, and indicate *p < 0.05, **p < 0.01.