The balance of metagenomic elements shapes the skin microbiome in acne and health.

Emma Barnard,Noah Craft,Baochen Shi,Dezhi Kang,Huiying Li

doi:10.1038/srep39491

Abstract

Studies have emphasized the importance of disease-associated microorganisms in perturbed communities, however, the protective roles of commensals are largely under recognized and poorly understood. Using acne as a model disease, we investigated the determinants of the overall virulence property of the skin microbiota when disease- and health-associated organisms coexist in the community. By ultra-deep metagenomic shotgun sequencing, we revealed higher relative abundances of propionibacteria and Propionibacterium acnes phage in healthy skin. In acne patients, the microbiome composition at the species level and at P. acnes strain level was more diverse than in healthy individuals, with enriched virulence-associated factors and reduced abundance of metabolic synthesis genes. Based on the abundance profiles of the metagenomic elements, we constructed a quantitative prediction model, which classified the clinical states of the host skin with high accuracy in both our study cohort (85%) and an independent sample set (86%). Our results suggest that the balance between metagenomic elements, not the mere presence of disease-associated strains, shapes the overall virulence property of the skin microbiota. This study provides new insights into the microbial mechanism of acne pathogenesis and suggests probiotic and phage therapies as potential acne treatments to modulate the skin microbiota and to maintain skin health.

Highlights

Studies have emphasized the importance of disease-associated microorganisms in perturbed communities, the protective roles of commensals are largely under recognized and poorly understood
In our previous characterization of the skin microbiome in healthy individuals and acne patients using 16S ribosomal RNA analysis, we revealed that certain P. acnes strains were highly associated with acne while some strains were associated with healthy skin[5]
After removal of human DNA sequences and low-quality reads, we obtained an average of 1.08 gigabase pairs (Gbp) per sample (6.9 × 107 bp – 4.8 × 109 bp), sufficient to cover the microbial diversity of skin samples[24]

Summary

Introduction

Studies have emphasized the importance of disease-associated microorganisms in perturbed communities, the protective roles of commensals are largely under recognized and poorly understood. Using acne as a model disease, we investigated the determinants of the overall virulence property of the skin microbiota when disease- and health-associated organisms coexist in the community. This study provides new insights into the microbial mechanism of acne pathogenesis and suggests probiotic and phage therapies as potential acne treatments to modulate the skin microbiota and to maintain skin health. As individuals often harbor multiple P. acnes strains simultaneously which may have different roles in disease or health, it is unclear how the colonization of multiple strains in the follicle may affect the overall virulence or health properties of the skin microbial community. Metagenomic shotgun sequencing analysis reveals the taxonomic composition and the functional potential of the microbiome, and can provide better understanding of the potential microbial involvement in health or disease at the molecular level.

Methods

Results

Conclusion