Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris

• Published in: Applied microbiology and biotechnology 2014-01, Vol.98 (1), p.411-424
• Main Authors: Wang, Yanhan, Kuo, Sherwin, Shu, Muya, Yu, Jinghua, Huang, Stephen, Dai, Ashley, Two, Aimee, Gallo, Richard L, Huang, Chun-Ming
• Format: Article
• Language: English
• Subjects: Abscesses; Acne; Acne Vulgaris - microbiology; Acne Vulgaris - therapy; Animals; Anti-Bacterial Agents - metabolism; Antibiosis; Antibiotics; Applied Microbial and Cell Physiology; Bacteria; Bacterial infections; Biological; Biomedical and Life Sciences; Biotechnology; Care and treatment; Causes of; Development and progression; DNA, Bacterial - chemistry; DNA, Bacterial - genetics; Drug resistance; Fatty acids; FDA approval; Fermentation; Genetic aspects; Glycerol; Glycerol - metabolism; Homeostasis; Human; human health; Humans; inflammation; Life Sciences; Mice; Microbial Genetics and Genomics; Microbiology; Microbiota (Symbiotic organisms); Microorganisms; Molecular Sequence Data; NMR; Nuclear magnetic resonance; nuclear magnetic resonance spectroscopy; pathogens; Physiological aspects; Probiotics; Probiotics - administration & dosage; Propionibacterium acnes; Propionibacterium acnes - drug effects; Propionibacterium acnes - growth & development; Propionibacterium acnes - physiology; Sequence Analysis, DNA; short chain fatty acids; Side effects; Skin - microbiology; Skin diseases; Staphylococcus; Staphylococcus epidermidis; Staphylococcus epidermidis - metabolism; Staphylococcus epidermidis - physiology; Staphylococcus infections; Studies; Succinic acid; Succinic Acid - metabolism; topical application
• ISSN: 0175-7598; 1432-0614
• DOI: 10.1007/s00253-013-5394-8

Increasing evidence demonstrates that commensal microorganisms in the human skin microbiome help fight pathogens and maintain homeostasis of the microbiome. However, it is unclear how these microorganisms maintain biological balance when one of them overgrows. The overgrowth of Propionibacterium acnes (P. acnes), a commensal skin bacterium, has been associated with the progression of acne vulgaris. Our results demonstrate that skin microorganisms can mediate fermentation of glycerol, which is naturally produced in skin, to enhance their inhibitory effects on P. acnes growth. The skin microorganisms, most of which have been identified as Staphylococcus epidermidis (S. epidermidis), in the microbiome of human fingerprints can ferment glycerol and create inhibition zones to repel a colony of overgrown P. acnes. Succinic acid, one of four short-chain fatty acids (SCFAs) detected in fermented media by nuclear magnetic resonance (NMR) analysis, effectively inhibits the growth of P. acnes in vitro and in vivo. Both intralesional injection and topical application of succinic acid to P. acnes-induced lesions markedly suppress the P. acnes-induced inflammation in mice. We demonstrate for the first time that bacterial members in the skin microbiome can undergo fermentation to rein in the overgrowth of P. acnes. The concept of bacterial interference between P. acnes and S. epidermidis via fermentation can be applied to develop probiotics against acne vulgaris and other skin diseases. In addition, it will open up an entirely new area of study for the biological function of the skin microbiome in promoting human health.