Challenges in exploring and manipulating the human skin microbiome

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Abstract

The skin is the exterior interface of the human body with the environment. Despite its harsh physical landscape, the skin is colonized by diverse commensal microbes. In this review, we discuss recent insights into skin microbial populations, including their composition and role in health and disease and their modulation by intrinsic and extrinsic factors, with a focus on the pathobiological basis of skin aging. We also describe the most recent tools for investigating the skin microbiota composition and microbe-skin relationships and perspectives regarding the challenges of skin microbiome manipulation.

Supplementary Information

The online version contains supplementary material available at 10.1186/s40168-021-01062-5.

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Most cited references 132

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Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.

M G Dominguez-Bello, E. Costello, M. Contreras … (2010)

Upon delivery, the neonate is exposed for the first time to a wide array of microbes from a variety of sources, including maternal bacteria. Although prior studies have suggested that delivery mode shapes the microbiota's establishment and, subsequently, its role in child health, most researchers have focused on specific bacterial taxa or on a single body habitat, the gut. Thus, the initiation stage of human microbiome development remains obscure. The goal of the present study was to obtain a community-wide perspective on the influence of delivery mode and body habitat on the neonate's first microbiota. We used multiplexed 16S rRNA gene pyrosequencing to characterize bacterial communities from mothers and their newborn babies, four born vaginally and six born via Cesarean section. Mothers' skin, oral mucosa, and vagina were sampled 1 h before delivery, and neonates' skin, oral mucosa, and nasopharyngeal aspirate were sampled <5 min, and meconium <24 h, after delivery. We found that in direct contrast to the highly differentiated communities of their mothers, neonates harbored bacterial communities that were undifferentiated across multiple body habitats, regardless of delivery mode. Our results also show that vaginally delivered infants acquired bacterial communities resembling their own mother's vaginal microbiota, dominated by Lactobacillus, Prevotella, or Sneathia spp., and C-section infants harbored bacterial communities similar to those found on the skin surface, dominated by Staphylococcus, Corynebacterium, and Propionibacterium spp. These findings establish an important baseline for studies tracking the human microbiome's successional development in different body habitats following different delivery modes, and their associated effects on infant health.

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The human skin microbiome

Allyson Byrd, Yasmine Belkaid, Julia A Segre (2018)

Functioning as the exterior interface of the human body with the environment, skin acts as a physical barrier to prevent the invasion of foreign pathogens while providing a home to the commensal microbiota. The harsh physical landscape of skin, particularly the desiccated, nutrient-poor, acidic environment, also contributes to the adversity that pathogens face when colonizing human skin. Despite this, the skin is colonized by a diverse microbiota. In this Review, we describe amplicon and shotgun metagenomic DNA sequencing studies that have been used to assess the taxonomic diversity of microorganisms that are associated with skin from the kingdom to the strain level. We discuss recent insights into skin microbial communities, including their composition in health and disease, the dynamics between species and interactions with the immune system, with a focus on Propionibacterium acnes, Staphylococcus epidermidis and Staphylococcus aureus.

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Topographical and temporal diversity of the human skin microbiome.

Elizabeth Grice, Heidi Kong, Sean Conlan … (2009)

Human skin is a large, heterogeneous organ that protects the body from pathogens while sustaining microorganisms that influence human health and disease. Our analysis of 16S ribosomal RNA gene sequences obtained from 20 distinct skin sites of healthy humans revealed that physiologically comparable sites harbor similar bacterial communities. The complexity and stability of the microbial community are dependent on the specific characteristics of the skin site. This topographical and temporal survey provides a baseline for studies that examine the role of bacterial communities in disease states and the microbial interdependencies required to maintain healthy skin.

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Author and article information

Contributors

Manon Boxberger: manon.boxberger@hotmail.fr

Valérie Cenizo: valerie.cenizo@loccitane.com

Nadim Cassir: cassirnadim@gmail.com

Bernard La Scola: bernard.la-scola@univ-amu.fr

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 30 May 2021

Publication date PMC-release: 30 May 2021

Publication date Collection: 2021

Volume: 9

Electronic Location Identifier: 125

Affiliations

[1 ]GRID grid.5399.6, ISNI 0000 0001 2176 4817, IRD, AP-HM, MEPHI, , Aix Marseille Université, ; Marseille, France

[2 ]GRID grid.483853.1, ISNI 0000 0004 0519 5986, IHU-Méditerranée Infection, ; 19-21 Boulevard Jean Moulin, 13385 Marseille Cedex 05, France

[3 ]Groupe L’Occitane, R&D Department, Zone Industrielle Saint Maurice, 4100 Manosque, Alpes-de Haute-Provence France

[4 ]GRID grid.5399.6, ISNI 0000 0001 2176 4817, IRD, AP-HM, SSA, VITROME, , Aix Marseille Université, ; Marseille, France

Article

Publisher ID: 1062

DOI: 10.1186/s40168-021-01062-5

PMC ID: 8166136

PubMed ID: 34053468

SO-VID: 6e1ace78-a340-48bc-8f3c-bebec5a29663

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 10 July 2020

Date accepted : 25 March 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;

Award ID: 10-1AHU-03

Funded by: FundRef http://dx.doi.org/10.13039/501100008530, European Regional Development Fund;

Award ID: PRIMI

Funded by: M&L Laboratories

Award ID: PVM :2018-200

Award Recipient : Manon Boxberger

Custom metadata

Keywords: skin,microbiome,bacteria,3d skin models,probiotics,cosmetics,diseases,culture,next-generation sequencing

Data availability:

Keywords: skin, microbiome, bacteria, 3d skin models, probiotics, cosmetics, diseases, culture, next-generation sequencing

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Challenges in exploring and manipulating the human skin microbiome

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Abstract

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Tick microbiome

Most cited references 132

Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.

The human skin microbiome

Topographical and temporal diversity of the human skin microbiome.

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