The dynamic balance of the skin microbiome across the lifespan

Abstract

For decades research has centered on identifying the ideal balanced skin microbiome that prevents disease and on developing therapeutics to foster this balance. However, this single idealized balance may not exist. The skin microbiome changes across the lifespan. This is reflected in the dynamic shifts of the skin microbiome's diverse, inter-connected community of microorganisms with age. While there are core skin microbial taxa, the precise community composition for any individual person is determined by local skin physiology, genetics, microbe-host interactions, and microbe-microbe interactions. As a key interface with the environment, the skin surface and its appendages are also constantly exchanging microbes with close personal contacts and the environment. Hormone fluctuations and immune system maturation also drive age-dependent changes in skin physiology that support different microbial community structures over time. Here, we review recent insights into the factors that shape the skin microbiome throughout life. Collectively, the works summarized within this review highlight how, depending on where we are in lifespan, our skin supports robust microbial communities, while still maintaining microbial features unique to us. This review will also highlight how disruptions to this dynamic microbial balance can influence risk for dermatological diseases as well as impact lifelong health.

Keywords: host–microbe interactions; microbiome; skin.

Figure 1.. The dynamic balance of the skin and its microbiome over the lifespan.

Over a lifetime the skin's physiology changes as an individual's cutaneous immune systems matures and hormones drive sweat and sebum gland development. These changes are associated with shifts in the relative abundance of prominent skin microbial taxa and shifts in the overall microbial community diversity. Microbiome data displays the average relative abundance of the top ten microbial taxa for each group as assessed by high-throughput sequencing of the bacterial 16S ribosomal RNA gene. Taxa with a relative abundance >20% in at least one group are bolded. Groups include newborns born either through vaginal delivery or cesarian section [22] as well as dry, moist, and sebaceous sites for infants (1 year old) [40], children (5 years old) [40], adolescents (Tanner Stage III) [46], adults (20–40 years old) [3], and the elderly (60 and older) [137]. Since sexual differences in skin microbial composition become more pronounced over the course of puberty [46], relative abundance plots for adolescent, adult, and elderly males and females are displayed. Inner circles represent relative microbial diversity, sebum production, sweat production, surface pH, skin integrity, and immune function throughout life [33,46,87,144,152,153].

Figure 2.. Differences in the skin, microbiome, and body odor production in early and late puberty.

In childhood and early puberty (Tanner Stages I to II) the skin microbiome is highly diverse and body odor is associated with CoNS (e.g., S. epidermidis and S. hominis) production of volatile fatty acids (e.g., propionic, acetic, and isovaleric acid; sour odors) and sulfur (rotten-egg odor) [92]. As puberty advances, steroid hormones promote sebaceous and apocrine sweat gland development [90,91], modify the types of lipids present in sebum [90,97], and enhance the skin barrier [94–96]. In later puberty (Tanner Stages IV to V), increased lipid production and altered lipid content is associated with a skin microbiome dominated by lipophilic taxa [46]. While breakdown of sweat and sebum components into volatile fatty acids still occurs, body odor in young adults becomes more associated with Corynebacterium spp. metabolism of sebum and sweat components into sulfanylalkanols (e.g., 3SH and 3M3SH; oniony odors), and volatile organic compounds (e.g., 3H3MHA; cumin like odors) [92,98–101]. BCAA: Branched chain amino acids; CGSC: Cystine-Glycine-S-conjugate; CoNS: Coagulase negative Staphylococcus spp.; GC: Glutaminyl-conjugate; 3H3MHA: 3-hydroxy-3-methylhexanoic acid; 3M3SH: 3-methyl-3-sullanylhexanol; 3SH: 3-sulfanylhexanol.