Background: Viruses play an essential role in the human skin microbiome under healthy and diseased conditions. We previously reported that exposure to polycyclic aromatic hydrocarbons (PAHs) led to the differentiation of bacteria samples from the cheeks of 124 Chinese women into two cutotypes with distinct taxonomic and functional compositions. In addition, we found that women with a high level of PAH exposure exhibited skin dryness and hyperpigmentation. However, the characteristics of viruses associated with these cutotypes are not well understood. In this study, we employed bulk metagenomic sequencing to investigate the diversity and functions of skin viromes and the virus–host interactions of the two cutotypes.
Results: The viruses associated with the two cutotypes had distinct diversities, compositions, functions, and lifestyles. Moreover, virus–host interactions were substantially increased by high levels of PAH exposure, especially when the hosts were potential pathogens. Under high- PAH exposure conditions, the viruses were enriched in xenobiotic degradation functions, and there was evidence suggesting that the insertion of bacteriophage-encoded auxiliary metabolic genes into hosts aids biodegradation. Furthermore, under low-PAH exposure conditions, virus– host interactions followed the “Piggyback-the-Winner” model, with Cutibacterium strains being “winners,” whereas under high-PAH exposure conditions, the interactions followed the “Piggyback-the-Persistent” model, with the biodegradation bacteria being “persistent.”
Conclusion: Our findings demonstrate that PAHs not only influence skin bacteria but also impact the composition of skin viruses and their interactions with skin bacteria, which may influence skin health. A detailed understanding of the roles played by viruses on skin exposed to air pollutants would aid the development of strategies to harness the potential of viruses to prevent undesirable skin conditions.