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

Marcus H Y Leung,Philippe Bastien,Arthur Tenenhaus,Lionel Breton,Nasrine Bourokba,Cécile Clavaud,Xinzhao Tong,Brice M R Appenzeller,Richard J Betts,Jing Li,Sakina Mezzache,Florent Guinot,Patrick K H Lee

doi:10.1186/s40168-020-00874-1

Abstract

BackgroundPolycyclic 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.ResultsSkin 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.ConclusionsThe 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.EdPNeYfwVemgFQnh9BH8shVideo

Highlights

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
An increased severity was observed in almost all facial signs, including wrinkles and pigmentation disorders, in individuals living in Baoding [10]
This study highlighted the potential roles pollutant exposure have on various aspects of the skin microbiota, including changes in diversity and abundances of taxa and alteration of the functional potentials that may be important for the commensal microbiota to protect the host against pathogens and maintain skin homeostasis

Summary

Introduction

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. Among the constituents of harmful atmospheric pollution, polycyclic aromatic hydrocarbons (PAHs), a class of organic pollutants in ambient air commonly associated with PM, may enter the human body and bloodstream via inhalation, ingestion, and dermal absorption [11,12,13]. While chronic dermal exposure to PAHs may be associated with premature skin aging, pigmentary disorder, acne, and skin cancer [10, 14, 15], the exact mechanisms by which PAH pollution harms the skin remain poorly understood and are likely to be complex and multifaceted

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