Biogeography and viability of bacteria in the skin microbiome and built environment

Abstract

Despite contributing to human health, fundamental aspects of the skin microbiome remain unclear. For example, the spatial organization of bacteria within skin and the viability of these bacteria are unknown. To address this, we applied culturing, imaging, and newly developed molecular approaches to human and mouse skin and found that the skin surface was colonized by fewer viable bacteria than predicted by bacterial DNA levels. Instead, viable bacteria were confined to hair follicles and other cutaneous structures. Furthermore, we showed that the skin microbiome had a uniquely low viability compared to other human microbiomes. Finally, we performed an in-vivo skin microbiome perturbation-recovery study using human volunteers. Bacterial 16S rRNA gene sequencing revealed that the skin microbiome was stable after perturbation and repopulation of the skin surface was driven by the underlying viable population. Our findings help explain the skin microbiome dynamics, as bacterial DNA on the skin surface can be transiently perturbed but is replenished by a stable, underlying, viable population. These results address outstanding questions in skin microbiome biology with implications for future efforts to study and manipulate it.This work also addresses bacterial viability in the built environment (BE), which consists of human-made structures. The BE microbiome can potentially affect human health because of the constant proximity to humans. This has led to increasing public concern of whether the bacteria in the BE are harmful. Previous studies have used sequencing-based approaches to assess the BE microbiome. However, the extent to which the bacterial DNA in the BE reflects infection potential remains unknown. To address this, we used culture-based and culture-independent methods to profile bacterial viability of the BE. We found that most bacterial DNA is not associated with viable bacteria. To understand the determinants of bacterial viability in the BE we used mock bacterial communities to investigate the effects of temperature, relative humidity, surface material, and human interaction. We found that relative humidity, temperature, and surface material did not have an effect, but environmental exposure decreased bacterial viability. These results update our conception of the BE microbiome and begin to define the factors that affect bacterial viability.