Skin microbiome: looking back to move forward

Heidi H Kong, Julia A Segre, Heidi H Kong, Julia A Segre

Abstract

Trillions of bacteria, fungi, viruses, archaea, and small arthropods colonize the skin surface, collectively comprising the skin microbiome. Generations of researchers have classified these microbes as transient versus resident, beneficial versus pathogenic, and collaborators versus adversaries. Culturing and direct sequencing of microbial inhabitants identified distinct populations present at skin surface sites. Herein, we explore the history of this field, describe findings from the current molecular sequencing era, and consider the future of investigating how microbes and antimicrobial therapy contribute to human health.

Figures

Figure 1. Schematic of skin histology viewed…
Figure 1. Schematic of skin histology viewed in cross-section with microorganisms and skin appendages
Microorganisms (virus, bacteria and fungi, mites) cover the surface of the skin and reside deep within the hair and glands.
Figure 2. Homonculus showing major sites and…
Figure 2. Homonculus showing major sites and range of Propionibacterium acnes colonization
Classic microbiologists swabbed and cultured diverse sites to characterize the predominant sites of colonization (“headquarters”) and general distribution (“range”). Adapted from Marples’ “The Ecology of the Human Skin”.
Figure 3. Topographical distribution of bacteria on…
Figure 3. Topographical distribution of bacteria on skin sites
The skin microbiome is highly dependent on the microenvironment of the sampled site. Sebaceous sites are labeled in blue, moist sites are labeled in green and dry surfaces are labeled in red. Family-level classification of bacteria colonizing an individual subject is shown. Data is from Grice et al, 2009.
Figure 4. Interpersonal variation of the skin…
Figure 4. Interpersonal variation of the skin microbiome
Characterization of the skin microbiota, as determined by 16S rRNA sequencing, of four sites on four healthy volunteers (HV1, HV2, HV3, HV4) is depicted. Skin microbial variation is more similar dependent on the site than the individual. A. Antecubital crease; B. Back; C. Nare; D. Plantar heel. Data from Grice et al, 2009.

References

    1. Allen AM, Taplin D. Tropical immersion foot. Lancet. 1973;2:1185–9.
    1. Capone KA, Dowd SE, Stamatas GN, Nikolovski J. Diversity of the human skin microbiome early in life. J Invest Dermatol. 2011;131:2026–32.
    1. Chiller K, Selkin BA, Murakawa GJ. Skin microflora and bacterial infections of the skin. J Investig Dermatol Symp Proc. 2001;6:170–4.
    1. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326:1694–7.
    1. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449:811–8.
    1. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4554–61.
    1. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971–5.
    1. Elias PM. Stratum corneum defensive functions: an integrated view. J Invest Dermatol. 2005;125:183–200.
    1. Fierer N, Hamady M, Lauber CL, Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A. 2008;105:17994–9.
    1. Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, Knight R. Forensic identification using skin bacterial communities. Proc Natl Acad Sci U S A. 2010;107:6477–81.
    1. Fredricks DN. Microbial ecology of human skin in health and disease. J Investig Dermatol Symp Proc. 2001;6:167–9.
    1. Gao Z, Tseng CH, Pei Z, Blaser MJ. Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci U S A. 2007;104:2927–32.
    1. Gao Z, Tseng CH, Strober BE, Pei Z, Blaser MJ. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE. 2008;3:e2719.
    1. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324:1190–2.
    1. Grice EA, Kong HH, Renaud G, Young AC, Bouffard GG, Blakesley RW, et al. A diversity profile of the human skin microbiota. Genome Res 2008
    1. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9:244–53.
    1. Grice EA, Snitkin ES, Yockey LJ, Bermudez DM, Liechty KW, Segre JA. Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. Proc Natl Acad Sci U S A. 2010;107:14799–804.
    1. Hanifin JM. Evolving concepts of pathogenesis in atopic dermatitis and other eczemas. J Invest Dermatol. 2009;129:320–2.
    1. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010;465:346–9.
    1. Kligman AM, Leyden JJ, McGinley KJ. Bacteriology. J Invest Dermatol. 1976;67:160–8.
    1. Kong HH. Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med. 2011;17:320–8.
    1. Lai Y, Cogen AL, Radek KA, Park HJ, Macleod DT, Leichtle A, et al. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol. 2010;130:2211–21.
    1. Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med. 2009;15:1377–82.
    1. Leyden JJ, McGinley KJ, Nordstrom KM, Webster GF. Skin microflora. J Invest Dermatol. 1987;88:65s–72s.
    1. Madison KC. Barrier function of the skin: “la raison d’etre” of the epidermis. J Invest Dermatol. 2003;121:231–41.
    1. Marples MJ. Life on the human skin. Sci Am. 1969;220:108–15.
    1. Marples RR, Downing DT, Kligman AM. Control of free fatty acids in human surface lipids by Corynebacterium acnes. J Invest Dermatol. 1971;56:127–31.
    1. Martin JM, Zenilman JM, Lazarus GS. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J Invest Dermatol. 2010;130:38–48.
    1. Noble WC. Skin Microblora and Microbial Skin Disease. Cambridge University Press; 1993.
    1. Otto M. Staphylococcus epidermidis--the ‘accidental’ pathogen. Nat Rev Microbiol. 2009;7:555–67.
    1. Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA, et al. The NIH Human Microbiome Project. Genome research. 2009;19:2317–23.
    1. Pillsbury DM, Kligman AM. Modern Trends in Dermatology, 2nd series. London: Butterworth; 1954. Some current problems in cutaneous bacteriology; pp. 187–213.
    1. Somerville DA, Seville RH, Cunningham RC, Noble WC, Savin JA. Erythrasma in a hospital for the mentally subnormal. Br J Dermatol. 1970;82:355–60.
    1. Taplin D, Bassett DC, Mertz PM. Foot lesions associated with Pseudomonas cepacia. Lancet. 1971;2:568–71.
    1. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449:804–10.
    1. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, et al. Vancomycinresistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest. 2010;120:4332–41.

Source: PubMed

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