TY - JOUR
T1 - Bacterial DNA on the skin surface overrepresents the viable skin microbiome
AU - Acosta, Ellen M.
AU - Little, Katherine A.
AU - Bratton, Benjamin P.
AU - Lopez, Jaime G.
AU - Mao, Xuming
AU - Payne, Aimee S.
AU - Donia, Mohamed
AU - Devenport, Danelle
AU - Gitai, Zemer
N1 - Funding Information:
We thank all members of the Gitai lab for their insights and comments. We also thank Dr. Gary Laevsky and the Princeton Molecular Biology Microscopy Core, which is a Nikon Center of Excellence, for microscopy support; Dr. Wei Wang and the Genomics Core Facility in The Lewis Sigler Institute for Integrative Genomics at Princeton University for support with 16S rRNA gene amplicon sequencing; Matthew Cahn for his assistance with processing 16S rRNA gene amplicon sequencing data; Bahar Javdan for processing the human fecal sample; Elizabeth Grice for support and feedback; and Laurice Flowers and Elizabeth Grice for providing the Staphylococcus epidermidis strain used. Funding was provided in part by NIH (DP1AI124669 to ZG, EMA, and BPB, and T32 GM007388 to EMA). Additional funding provided by the National Science Foundation (NSF PHY-1734030 to BPB). Research reported in this publication was also supported by the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number TL1TR003019 (EMA) and by the Schmidt Transformative Technology Fund (EMA). This work was supported in part by the Penn Skin Biology and Diseases Resource-based Center (P30-AR068589) and the University of Pennsylvania Perelman School of Medicine. The contents are solely the responsibility of the authors and do not necessarily represent the official views of the respective funding agencies.
Publisher Copyright:
© 2023, eLife Sciences Publications Ltd. All rights reserved.
PY - 2023/6
Y1 - 2023/6
N2 - The skin microbiome provides vital contributions to human health. However, the spatial organization and viability of its bacterial components remain unclear. Here, we apply culturing, imaging, and molecular approaches to human and mouse skin samples, and find that the skin surface is colonized by fewer viable bacteria than predicted by bacterial DNA levels. Instead, viable skin-associated bacteria are predominantly located in hair follicles and other cutaneous invaginations. Furthermore, we show that the skin microbiome has a uniquely low fraction of viable bacteria compared to other human microbiome sites, indicating that most bacterial DNA on the skin surface is not associated with viable cells Additionally, a small number of bacterial families dominate each skin site and traditional sequencing methods overestimate both the richness and diversity of the skin microbiome. Finally, we performed an in vivo skin microbiome perturbation-recovery study using human volunteers. Bacterial 16S rRNA gene sequencing revealed that, while the skin microbiome is remarkably stable even in the wake of aggressive perturbation, repopulation of the skin surface is driven by the underlying viable population. Our findings help explain the dynamics of skin microbiome perturbation as bacterial DNA on the skin surface can be transiently perturbed but is replenished by a stable underlying viable population. These results address multiple outstanding questions in skin microbiome biology with significant implications for future efforts to study and manipulate it.
AB - The skin microbiome provides vital contributions to human health. However, the spatial organization and viability of its bacterial components remain unclear. Here, we apply culturing, imaging, and molecular approaches to human and mouse skin samples, and find that the skin surface is colonized by fewer viable bacteria than predicted by bacterial DNA levels. Instead, viable skin-associated bacteria are predominantly located in hair follicles and other cutaneous invaginations. Furthermore, we show that the skin microbiome has a uniquely low fraction of viable bacteria compared to other human microbiome sites, indicating that most bacterial DNA on the skin surface is not associated with viable cells Additionally, a small number of bacterial families dominate each skin site and traditional sequencing methods overestimate both the richness and diversity of the skin microbiome. Finally, we performed an in vivo skin microbiome perturbation-recovery study using human volunteers. Bacterial 16S rRNA gene sequencing revealed that, while the skin microbiome is remarkably stable even in the wake of aggressive perturbation, repopulation of the skin surface is driven by the underlying viable population. Our findings help explain the dynamics of skin microbiome perturbation as bacterial DNA on the skin surface can be transiently perturbed but is replenished by a stable underlying viable population. These results address multiple outstanding questions in skin microbiome biology with significant implications for future efforts to study and manipulate it.
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U2 - 10.7554/eLife.87192
DO - 10.7554/eLife.87192
M3 - Article
C2 - 37389570
AN - SCOPUS:85164232729
SN - 2050-084X
VL - 12
JO - eLife
JF - eLife
M1 - RP87192
ER -