Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants

Abstract Background Polycyclic aromatic hydrocarbons (PAHs) are of environmental and public health concerns and contribute to adverse skin attributes such as premature skin aging and pigmentary disorder. However, little information is available on the potential roles of chronic urban PAH pollutant e...

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Main Authors: Marcus H. Y. Leung, Xinzhao Tong, Philippe Bastien, Florent Guinot, Arthur Tenenhaus, Brice M. R. Appenzeller, Richard J. Betts, Sakina Mezzache, Jing Li, Nasrine Bourokba, Lionel Breton, Cécile Clavaud, Patrick K. H. Lee
Format: Article
Language:English
Published: BMC 2020-06-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-020-00874-1
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spelling doaj-4138d6a8d9f345fcbdcfed4ddd0b7fd52020-11-25T03:12:35ZengBMCMicrobiome2049-26182020-06-018111710.1186/s40168-020-00874-1Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutantsMarcus H. Y. Leung0Xinzhao Tong1Philippe Bastien2Florent Guinot3Arthur Tenenhaus4Brice M. R. Appenzeller5Richard J. Betts6Sakina Mezzache7Jing Li8Nasrine Bourokba9Lionel Breton10Cécile Clavaud11Patrick K. H. Lee12School of Energy and Environment, City University of Hong KongSchool of Energy and Environment, City University of Hong KongL’Oréal Research and InnovationL’Oréal Research and InnovationCentraleSupelec-L2S-Laboratoire des signaux et systèmes, Brain and Spine Institute, Université Paris-SudHuman Biomonitoring Research Unit, Luxembourg Institute of HealthL’Oréal Research and InnovationL’Oréal Research and InnovationL’Oréal Research and InnovationL’Oréal Research and InnovationL’Oréal Research and InnovationL’Oréal Research and InnovationSchool of Energy and Environment, City University of Hong KongAbstract Background Polycyclic aromatic hydrocarbons (PAHs) are of environmental and public health concerns and contribute to adverse skin attributes such as premature skin aging and pigmentary disorder. However, little information is available on the potential roles of chronic urban PAH pollutant exposure on the cutaneous microbiota. Given the roles of the skin microbiota have on healthy and undesirable skin phenotypes and the relationships between PAHs and skin properties, we hypothesize that exposure of PAHs may be associated with changes in the cutaneous microbiota. In this study, the skin microbiota of over two hundred Chinese individuals from two cities in China with varying exposure levels of PAHs were characterized by bacterial and fungal amplicon and shotgun metagenomics sequencing. Results Skin site and city were strong parameters in changing microbial communities and their assembly processes. Reductions of bacterial-fungal microbial network structural integrity and stability were associated with skin conditions (acne and dandruff). Multivariate analysis revealed associations between abundances of Propionibacterium and Malassezia with host properties and pollutant exposure levels. Shannon diversity increase was correlated to exposure levels of PAHs in a dose-dependent manner. Shotgun metagenomics analysis of samples (n = 32) from individuals of the lowest and highest exposure levels of PAHs further highlighted associations between the PAHs quantified and decrease in abundances of skin commensals and increase in oral bacteria. Functional analysis identified associations between levels of PAHs and abundance of microbial genes of metabolic and other pathways with potential importance in host-microbe interactions as well as degradation of aromatic compounds. Conclusions The results in this study demonstrated the changes in composition and functional capacities of the cutaneous microbiota associated with chronic exposure levels of PAHs. Findings from this study will aid the development of strategies to harness the microbiota in protecting the skin against pollutants. Video Abstracthttp://link.springer.com/article/10.1186/s40168-020-00874-1Skin microbiotaSequencingUrban pollutionPolycyclic aromatic hydrocarbons
collection DOAJ
language English
format Article
sources DOAJ
author Marcus H. Y. Leung
Xinzhao Tong
Philippe Bastien
Florent Guinot
Arthur Tenenhaus
Brice M. R. Appenzeller
Richard J. Betts
Sakina Mezzache
Jing Li
Nasrine Bourokba
Lionel Breton
Cécile Clavaud
Patrick K. H. Lee
spellingShingle Marcus H. Y. Leung
Xinzhao Tong
Philippe Bastien
Florent Guinot
Arthur Tenenhaus
Brice M. R. Appenzeller
Richard J. Betts
Sakina Mezzache
Jing Li
Nasrine Bourokba
Lionel Breton
Cécile Clavaud
Patrick K. H. Lee
Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
Microbiome
Skin microbiota
Sequencing
Urban pollution
Polycyclic aromatic hydrocarbons
author_facet Marcus H. Y. Leung
Xinzhao Tong
Philippe Bastien
Florent Guinot
Arthur Tenenhaus
Brice M. R. Appenzeller
Richard J. Betts
Sakina Mezzache
Jing Li
Nasrine Bourokba
Lionel Breton
Cécile Clavaud
Patrick K. H. Lee
author_sort Marcus H. Y. Leung
title Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
title_short Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
title_full Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
title_fullStr Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
title_full_unstemmed Changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
title_sort changes of the human skin microbiota upon chronic exposure to polycyclic aromatic hydrocarbon pollutants
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2020-06-01
description Abstract Background Polycyclic aromatic hydrocarbons (PAHs) are of environmental and public health concerns and contribute to adverse skin attributes such as premature skin aging and pigmentary disorder. However, little information is available on the potential roles of chronic urban PAH pollutant exposure on the cutaneous microbiota. Given the roles of the skin microbiota have on healthy and undesirable skin phenotypes and the relationships between PAHs and skin properties, we hypothesize that exposure of PAHs may be associated with changes in the cutaneous microbiota. In this study, the skin microbiota of over two hundred Chinese individuals from two cities in China with varying exposure levels of PAHs were characterized by bacterial and fungal amplicon and shotgun metagenomics sequencing. Results Skin site and city were strong parameters in changing microbial communities and their assembly processes. Reductions of bacterial-fungal microbial network structural integrity and stability were associated with skin conditions (acne and dandruff). Multivariate analysis revealed associations between abundances of Propionibacterium and Malassezia with host properties and pollutant exposure levels. Shannon diversity increase was correlated to exposure levels of PAHs in a dose-dependent manner. Shotgun metagenomics analysis of samples (n = 32) from individuals of the lowest and highest exposure levels of PAHs further highlighted associations between the PAHs quantified and decrease in abundances of skin commensals and increase in oral bacteria. Functional analysis identified associations between levels of PAHs and abundance of microbial genes of metabolic and other pathways with potential importance in host-microbe interactions as well as degradation of aromatic compounds. Conclusions The results in this study demonstrated the changes in composition and functional capacities of the cutaneous microbiota associated with chronic exposure levels of PAHs. Findings from this study will aid the development of strategies to harness the microbiota in protecting the skin against pollutants. Video Abstract
topic Skin microbiota
Sequencing
Urban pollution
Polycyclic aromatic hydrocarbons
url http://link.springer.com/article/10.1186/s40168-020-00874-1
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