Universal Dermal Microbiome in Human Skin

Abstract

Human skin microbiota has been described as a "microbial fingerprint" due to observed differences between individuals. Current understanding of the cutaneous microbiota is based on sampling the outermost layers of the epidermis, while the microbiota in the remaining skin layers has not yet been fully characterized. Environmental conditions can vary drastically between the cutaneous compartments and give rise to unique communities. We demonstrate that the dermal microbiota is surprisingly similar among individuals and contains a specific subset of the epidermal microbiota. Variability in bacterial community composition decreased significantly from the epidermal to the dermal compartment but was similar among anatomic locations (hip and knee). The composition of the epidermal microbiota was more strongly affected by environmental factors than that of the dermal community. These results indicate a well-conserved dermal community that is functionally distinct from the epidermal community, challenging the current dogma. Future studies in cutaneous disorders and chronic infections may benefit by focusing on the dermal microbiota as a persistent microbial community.IMPORTANCE Human skin microbiota is thought to be unique according to the individual's lifestyle and genetic predisposition. This is true for the epidermal microbiota, while our findings demonstrate that the dermal microbiota is universal between healthy individuals. The preserved dermal microbial community is compositionally unique and functionally distinct to the specific environment in the depth of human skin. It is expected to have direct contact with the immune response of the human host, and research in the communication between host and microbiota should be targeted to this cutaneous compartment. This novel insight into specific microbial adaptation can be used advantageously in the research of chronic disorders and infections of the skin. It can enlighten the alteration between health and disease to the benefit of patients suffering from long-lasting socioeconomic illnesses.

Keywords: 16S rRNA genes; DNA sequencing; cutaneous compartments; dermal microbiota; dry habitat; skin biopsies; skin microbiome.

FIG 1

Bacterial composition in box plot and NMDS plot. (a) OTU richness by anatomic location (hip versus knee) and skin compartment (epidermal versus dermal). There were no differences in OTU richness between hip and knee. OTU richness increased from the dermal to the epidermal compartment. (b) An NMDS plot of bacterial 16S composition with clear grouping by skin location. Skin compartment and anatomic location are represented by point color and shape, respectively, while dotted lines represent a 95% reference interval for the skin compartment.

FIG 2

Heat tree illustrating the overall taxonomy of the bacterial community across the dermal compartment relative to that of the epidermal compartment (see the supplemental information). Color changes represent the difference in log₂ ratio of median proportions of reads between epidermal and dermal compartments. The blue nodes are more enriched in the epidermal compartment, while yellow nodes are more enriched in the dermal compartment. The gray nodes are equally present in both compartments.

FIG 3

Persistence plot. The persistence of 75 genera/species that differ significantly in persistence between the dermal and epidermal compartments. They are grouped according to their anaerobic or aerobic preference and their presence in both the epidermal and dermal compartments or in the epidermal compartment only. Of the genera/species significantly different in persistence between the two compartments, 61% were aerobic and 39% were anaerobic. Among the genera/species present only in the epidermal compartment, 35% were aerobic and 65% were anaerobic.

FIG 4

Heat map and ridge plot of predicted pathways. Predicted relative abundances of the pathways that differ the most between dermal (blue) and epidermal (black) compartments (all q values < 0.05). (a) (a) Heat map of log Z-scores of relative abundances visualized in blue (enriched) to yellow (depleted); (b) kernel density plots of differences between dermal and epidermal compartments from all paired samples. Trees are built with hierarchical clustering.