Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The skin microbiome

A Corrigendum to this article was published on 27 June 2011

This article has been updated

Key Points

  • The skin is a physical barrier against invasion by pathogenic organisms and foreign substances. The skin is also an ecosystem, host to a microbial milieu that, for the most part, is harmless.

  • The habitat of the skin varies topographically and is likely to be associated with variation in the colonizing microbiota. Factors contributing to variation in the skin microbiota include the density of hair follicles and glands (sweat or sebaceous), host factors (such as age and sex) and environmental factors (such as occupation, climate and hygiene).

  • Analysing skin bacterial microbiota by sequencing of 16S ribosomal RNA genes reveals a greater diversity of organisms than has been found by culture-based methods.

  • The microenvironment of the skin site sampled determines to a large extent the colonization by the predominant species, the temporal variation and the interpersonal variation. Propionibacterium spp. predominate in sebaceous areas, Corynebacterium and Staphylococcus spp. predominate in moist areas, and dry areas exhibit the greatest amount of diversity.

  • Compared with other mucosal microbiomes, the skin microbiome shows the greatest variability over time and harbours the greatest phylogenetic diversity.

  • The cutaneous immune system modulates colonization by the microbiota and is also vital during infection and wounding. Dysregulation of the skin immune response is evident in several skin disorders.

  • A wide range of skin disorders are postulated to arise in part owing to a microbial component. These disorders include atopic dermatitis, acne, seborrhoeic dermatitis and chronic wounds. Additionally, commensal bacteria (for example, Staphylococcus epidermidis) can become pathogenic and cause invasive infection.

Abstract

The skin is the human body's largest organ, colonized by a diverse milieu of microorganisms, most of which are harmless or even beneficial to their host. Colonization is driven by the ecology of the skin surface, which is highly variable depending on topographical location, endogenous host factors and exogenous environmental factors. The cutaneous innate and adaptive immune responses can modulate the skin microbiota, but the microbiota also functions in educating the immune system. The development of molecular methods to identify microorganisms has led to an emerging view of the resident skin bacteria as highly diverse and variable. An enhanced understanding of the skin microbiome is necessary to gain insight into microbial involvement in human skin disorders and to enable novel promicrobial and antimicrobial therapeutic approaches for their treatment.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic of skin histology viewed in cross-section with microorganisms and skin appendages.
Figure 2: Factors contributing to variation in the skin microbiome.
Figure 3: Topographical distribution of bacteria on skin sites.
Figure 4: Interpersonal variation of the skin microbiome.

Similar content being viewed by others

Change history

  • 27 June 2011

    It has been brought to our attention that in FIG. 1 of the original article the morphology and localization of the Demodex mites were not accurate. We have corrected the figure to show a cartoon that is more representative of the straight body and short limbs of these mites, and of their localization in the hair follicle. The correct figure is now shown. We thank I. Dekio for bringing this to our attention and apologize to readers for any confusion caused.

References

  1. Chiller, K., Selkin, B. A. & Murakawa, G. J. Skin microflora and bacterial infections of the skin. J. Investig. Dermatol. Symp. Proc. 6, 170–174 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Fredricks, D. N. Microbial ecology of human skin in health and disease. J. Investig. Dermatol. Symp. Proc. 6, 167–169 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Marples, M. The Ecology of the Human Skin (Charles C Thomas, Bannerstone House, Springfield, Illinois, 1965). A seminal and comprehensive work of classical dermatological microbiology.

    Google Scholar 

  4. Roth, R. R. & James, W. D. Microbial ecology of the skin. Annu. Rev. Microbiol. 42, 441–464 (1988).

    Article  CAS  PubMed  Google Scholar 

  5. Noble, W. C. Skin microbiology: coming of age. J. Med. Microbiol. 17, 1–12 (1984).

    Article  CAS  PubMed  Google Scholar 

  6. Roth, R. R. & James, W. D. Microbiology of the skin: resident flora, ecology, infection. J. Am. Acad. Dermatol. 20, 367–390 (1989).

    Article  CAS  PubMed  Google Scholar 

  7. Cogen, A. L., Nizet, V. & Gallo, R. L. Skin microbiota: a source of disease or defence? Br. J. Dermatol. 158, 442–455 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tagami, H. Location-related differences in structure and function of the stratum corneum with special emphasis on those of the facial skin. Int. J. Cosmet Sci. 30, 413–434 (2008).

    Article  CAS  PubMed  Google Scholar 

  9. Proksch, E., Brandner, J. M. & Jensen, J. M. The skin: an indispensable barrier. Exp. Dermatol. 17, 1063–1072 (2008).

    Article  PubMed  Google Scholar 

  10. Elias, P. M. The skin barrier as an innate immune element. Semin. Immunopathol. 29, 3–14 (2007).

    Article  PubMed  Google Scholar 

  11. Segre, J. A. Epidermal barrier formation and recovery in skin disorders. J. Clin. Invest. 116, 1150–1158 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fuchs, E. & Raghavan, S. Getting under the skin of epidermal morphogenesis. Nature Rev. Genet. 3, 199–209 (2002).

    Article  CAS  PubMed  Google Scholar 

  13. Leeming, J. P., Holland, K. T. & Cunliffe, W. J. The microbial ecology of pilosebaceous units isolated from human skin. J. Gen. Microbiol. 130, 803–807 (1984).

    CAS  PubMed  Google Scholar 

  14. Cohn, B. A. In search of human skin pheromones. Arch. Dermatol. 130, 1048–1051 (1994).

    Article  CAS  PubMed  Google Scholar 

  15. Emter, R. & Natsch, A. The sequential action of a dipeptidase and a β-lyase is required for the release of the human body odorant 3-methyl-3-sulfanylhexan-1-ol from a secreted Cys-Gly-(S) conjugate by Corynebacteria. J. Biol. Chem. 283, 20645–20652 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Decreau, R. A., Marson, C. M., Smith, K. E. & Behan, J. M. Production of malodorous steroids from androsta-5,16-dienes and androsta-4,16-dienes by Corynebacteria and other human axillary bacteria. J. Steroid Biochem. Mol. Biol. 87, 327–336 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Martin, A. et al. A functional ABCC11 allele is essential in the biochemical formation of human axillary odor. J. Invest. Dermatol. 130, 529–540 (2010).

    Article  CAS  PubMed  Google Scholar 

  18. Natsch, A., Gfeller, H., Gygax, P., Schmid, J. & Acuna, G. A specific bacterial aminoacylase cleaves odorant precursors secreted in the human axilla. J. Biol. Chem. 278, 5718–5727 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. Bruggemann, H. et al. The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305, 671–673 (2004).

    Article  CAS  PubMed  Google Scholar 

  20. Marples, R. R., Downing, D. T. & Kligman, A. M. Control of free fatty acids in human surface lipids by Corynebacterium acnes. J. Invest. Dermatol. 56, 127–131 (1971).

    Article  CAS  PubMed  Google Scholar 

  21. Ingham, E., Holland, K. T., Gowland, G. & Cunliffe, W. J. Partial purification and characterization of lipase (EC 3.1.1.3) from Propionibacterium acnes. J. Gen. Microbiol. 124, 393–401 (1981).

    CAS  PubMed  Google Scholar 

  22. Gribbon, E. M., Cunliffe, W. J. & Holland, K. T. Interaction of Propionibacterium acnes with skin lipids in vitro. J. Gen. Microbiol. 139, 1745–1751 (1993).

    Article  CAS  PubMed  Google Scholar 

  23. Korting, H. C., Hubner, K., Greiner, K., Hamm, G. & Braun-Falco, O. Differences in the skin surface pH and bacterial microflora due to the long-term application of synthetic detergent preparations of pH 5.5 and pH 7.0. Results of a crossover trial in healthy volunteers. Acta Derm. Venereol. 70, 429–431 (1990).

    CAS  PubMed  Google Scholar 

  24. Aly, R., Shirley, C., Cunico, B. & Maibach, H. I. Effect of prolonged occlusion on the microbial flora, pH, carbon dioxide and transepidermal water loss on human skin. J. Invest. Dermatol. 71, 378–381 (1978).

    Article  CAS  PubMed  Google Scholar 

  25. Hentges, D. J. The anaerobic microflora of the human body. Clin. Infect. Dis. 16, S175–S180 (1993).

    Article  PubMed  Google Scholar 

  26. Webster, G. F., Ruggieri, M. R. & McGinley, K. J. Correlation of Propionibacterium acnes populations with the presence of triglycerides on nonhuman skin. Appl. Environ. Microbiol. 41, 1269–1270 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Leyden, J. J., McGinley, K. J., Mills, O. H. & Kligman, A. M. Age-related changes in the resident bacterial flora of the human face. J. Invest. Dermatol. 65, 379–381 (1975).

    Article  CAS  PubMed  Google Scholar 

  28. Somerville, D. A. The normal flora of the skin in different age groups. Br. J. Dermatol. 81, 248–258 (1969).

    Article  CAS  PubMed  Google Scholar 

  29. Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci. USA 107, 11971–11975 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sarkany, I. & Gaylarde, C. C. Bacterial colonisation of the skin of the newborn. J. Pathol. Bacteriol. 95, 115–122 (1968).

    Article  CAS  PubMed  Google Scholar 

  31. Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Marples, R. R. Sex, constancy, and skin bacteria. Arch. Dermatol. Res. 272, 317–320 (1982).

    Article  CAS  PubMed  Google Scholar 

  33. Fierer, N., Hamady, M., Lauber, C. L. & Knight, R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc. Natl Acad. Sci. USA 105, 17994–17999 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Giacomoni, P. U., Mammone, T. & Teri, M. Gender-linked differences in human skin. J. Dermatol. Sci. 55, 144–149 (2009).

    Article  CAS  Google Scholar 

  35. Dethlefsen, L. & Relman, D. A. Microbes and Health Sackler Colloquium: Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. USA 16 Sep 2010 (doi:10.1073/pnas.1000087107).

    Article  Google Scholar 

  36. Antonopoulos, D. A. et al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 77, 2367–2375 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dethlefsen, L., Huse, S., Sogin, M. L. & Relman, D. A. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6, e280 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. McBride, M. E., Duncan, W. C. & Knox, J. M. The environment and the microbial ecology of human skin. Appl. Environ. Microbiol. 33, 603–608 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Faergemann, J. & Larko, O. The effect of UV-light on human skin microorganisms. Acta Derm. Venereol. 67, 69–72 (1987).

    CAS  PubMed  Google Scholar 

  40. Gao, Z., Tseng, C. H., Pei, Z. & Blaser, M. J. Molecular analysis of human forearm superficial skin bacterial biota. Proc. Natl Acad. Sci. USA 104, 2927–2932 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Grice, E. A. et al. A diversity profile of the human skin microbiota. Genome Res. 18, 1043–1050 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Grice, E. A. et al. Topographical and temporal diversity of the human skin microbiome. Science 324, 1190–1192 (2009). A comprehensive analysis of skin microbiota across 20 sites.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Costello, E. K. et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 (2009). A comprehensive analysis of skin, gut and oral microbiota in the same individuals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Eckburg, P. B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635–1638 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Dewhirst, F. E. et al. The human oral microbiome. J. Bacteriol. 192, 5002–5017 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zaura, E., Keijser, B. J., Huse, S. M. & Crielaard, W. Defining the healthy 'core microbiome' of oral microbial communities. BMC Microbiol. 9, 259 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Bik, E. M. et al. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 4, 962–974 (2010).

    Article  PubMed  Google Scholar 

  48. Pei, Z. et al. Bacterial biota in the human distal esophagus. Proc. Natl Acad. Sci. USA 101, 4250–4255 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bik, E. M. et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl Acad. Sci. USA 103, 732–737 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Leyden, J. J., McGinley, K. J., Holzle, E., Labows, J. N. & Kligman, A. M. The microbiology of the human axilla and its relationship to axillary odor. J. Invest. Dermatol. 77, 413–416 (1981).

    Article  CAS  PubMed  Google Scholar 

  51. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006). An important study demonstrating the functional potential of the human microbiome.

    Article  PubMed  Google Scholar 

  52. James, T. Y. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818–822 (2006).

    Article  CAS  PubMed  Google Scholar 

  53. Chase, M. W. & Fay, M. F. Ecology. Barcoding of plants and fungi. Science 325, 682–683 (2009).

    Article  CAS  PubMed  Google Scholar 

  54. Paulino, L. C., Tseng, C. H. & Blaser, M. J. Analysis of Malassezia microbiota in healthy superficial human skin and in psoriatic lesions by multiplex real-time PCR. FEMS Yeast Res. 8, 460–471 (2008).

    Article  CAS  PubMed  Google Scholar 

  55. Paulino, L. C., Tseng, C. H., Strober, B. E. & Blaser, M. J. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J. Clin. Microbiol 44, 2933–2941 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Gao, Z., Perez-Perez, G. I., Chen, Y. & Blaser, M. J. Quantitation of major human cutaneous bacterial and fungal populations. J. Clin. Microbiol. 48, 3575–3581 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Peleg, A. Y., Hogan, D. A. & Mylonakis, E. Medically important bacterial-fungal interactions. Nature Rev. Microbiol. 8, 340–349 (2010). This review describes the clinical and molecular characteristics of bacterium–fungus interactions that are relevant to human disease with a focus on Candida spp..

    Article  CAS  Google Scholar 

  58. Lacey, N., Delaney, S., Kavanagh, K. & Powell, F. C. Mite-related bacterial antigens stimulate inflammatory cells in rosacea. Br. J. Dermatol. 157, 474–481 (2007).

    Article  CAS  PubMed  Google Scholar 

  59. Georgala, S. et al. Increased density of Demodex folliculorum and evidence of delayed hypersensitivity reaction in subjects with papulopustular rosacea. J. Eur. Acad. Dermatol. Venereol. 15, 441–444 (2001).

    Article  CAS  PubMed  Google Scholar 

  60. Elston, D. M. Demodex mites: facts and controversies. Clin. Dermatol. 28, 502–504 (2010).

    Article  PubMed  Google Scholar 

  61. Hay, R. Demodex and skin infection: fact or fiction. Curr. Opin. Infect. Dis. 23, 103–105 (2010).

    Article  PubMed  Google Scholar 

  62. Schowalter, R. M., Pastrana, D. V., Pumphrey, K. A., Moyer, A. L. & Buck, C. B. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7, 509–515 (2010). An investigation of the preponderance of Merkel cell polyomavirus, and a methodology to isolate circular DNA viral genomes from human skin swabs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Borkowski, A. W. & Gallo, R. L. The coordinated response of the physical and antimicrobial peptide barriers of the skin. J. Invest. Dermatol. 131, 285–287 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Braff, M. H., Bardan, A., Nizet, V. & Gallo, R. L. Cutaneous defence mechanisms by antimicrobial peptides. J. Invest. Dermatol. 125, 9–13 (2005).

    Article  CAS  PubMed  Google Scholar 

  65. Strober, W. Epithelial cells pay a Toll for protection. Nature Med. 10, 898–900 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Fukao, T. & Koyasu, S. PI3K and negative regulation of TLR signaling. Trends Immunol. 24, 358–363 (2003).

    Article  CAS  PubMed  Google Scholar 

  67. Cogen, A. L. et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J. Invest. Dermatol. 130, 192–200 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cogen, A. L. et al. Staphylococcus epidermidis antimicrobial δ -toxin (phenol-soluble modulin-γ) cooperates with host antimicrobial peptides to kill Group A Streptococcus. PLoS ONE 5, e8557 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lai, Y. et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nature Med. 15, 1377–1382 (2009). This analysis demonstrated that products of a skin commensal can modulate the innate immune response.

    Article  CAS  PubMed  Google Scholar 

  70. Lai, Y. et al. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defence against bacterial skin infections. J. Invest. Dermatol. 130, 2211–2221 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Nomura, I. et al. Distinct patterns of gene expression in the skin lesions of atopic dermatitis and psoriasis: a gene microarray analysis. J. Allergy Clin. Immunol. 112, 1195–1202 (2003).

    Article  CAS  PubMed  Google Scholar 

  72. Nomura, I. et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J. Immunol. 171, 3262–3269 (2003).

    Article  CAS  PubMed  Google Scholar 

  73. Gudjonsson, J. E. et al. Global gene expression analysis reveals evidence for decreased lipid biosynthesis and increased innate immunity in uninvolved psoriatic skin. J. Invest. Dermatol. 129, 2795–2804 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ong, P. Y. et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347, 1151–1160 (2002).

    Article  CAS  PubMed  Google Scholar 

  75. de Jongh, G. J. et al. High expression levels of keratinocyte antimicrobial proteins in psoriasis compared with atopic dermatitis. J. Invest. Dermatol. 125, 1163–1173 (2005).

    Article  CAS  PubMed  Google Scholar 

  76. Owen, C. M., Chalmers, R. J., O'Sullivan, T. & Griffiths, C. E. A systematic review of antistreptococcal interventions for guttate and chronic plaque psoriasis. Br. J. Dermatol. 145, 886–890 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Pierard, G. E., Arrese, J. E., Pierard-Franchimont, C. & De Doncker, P. Prolonged effects of antidandruff shampoos — time to recurrence of Malassezia ovalis colonization of skin. Int. J. Cosmet. Sci. 19, 111–117 (1997).

    Article  CAS  PubMed  Google Scholar 

  78. Leyden, J. J., McGinley, K. J. & Kligman, A. M. Role of microorganisms in dandruff. Arch. Dermatol. 112, 333–338 (1976).

    Article  CAS  PubMed  Google Scholar 

  79. Gupta, A. K., Batra, R., Bluhm, R., Boekhout, T. & Dawson, T. L. Jr. Skin diseases associated with Malassezia species. J. Am. Acad. Dermatol. 51, 785–798 (2004).

    Article  PubMed  Google Scholar 

  80. Dessinioti, C. & Katsambas, A. D. The role of Propionibacterium acnes in acne pathogenesis: facts and controversies. Clin. Dermatol. 28, 2–7 (2010).

    Article  PubMed  Google Scholar 

  81. Scott, D. G., Cunliffe, W. J. & Gowland, G. Activation of complement — a mechanism for the inflammation in acne. Br. J. Dermatol. 101, 315–320 (1979).

    Article  CAS  PubMed  Google Scholar 

  82. Webster, G. F., Leyden, J. J. & Nilsson, U. R. Complement activation in acne vulgaris: consumption of complement by comedones. Infect. Immun. 26, 183–186 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Jeremy, A. H., Holland, D. B., Roberts, S. G., Thomson, K. F. & Cunliffe, W. J. Inflammatory events are involved in acne lesion initiation. J. Invest. Dermatol. 121, 20–27 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Kim, J. Review of the innate immune response in acne vulgaris: activation of Toll-like receptor 2 in acne triggers inflammatory cytokine responses. Dermatology 211, 193–198 (2005).

    Article  CAS  PubMed  Google Scholar 

  85. Puhvel, S. M. & Sakamoto, M. Cytotaxin production by comedonal bacteria (Propionibacterium acnes, Propionibacterium granulosum and Staphylococcus epidermidis). J. Invest. Dermatol. 74, 36–39 (1980).

    Article  CAS  PubMed  Google Scholar 

  86. Webster, G. F. & Leyden, J. J. Characterization of serum-independent polymorphonuclear leukocyte chemotactic factors produced by Propionibacterium acnes. Inflammation 4, 261–269 (1980).

    Article  CAS  PubMed  Google Scholar 

  87. Bek-Thomsen, M., Lomholt, H. B. & Kilian, M. Acne is not associated with yet-uncultured bacteria. J. Clin. Microbiol. 46, 3355–3360 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Hanifin, J. M. & Rogge, J. L. Staphylococcal infections in patients with atopic dermatitis. Arch. Dermatol. 113, 1383–1386 (1977).

    Article  CAS  PubMed  Google Scholar 

  89. Leyden, J. J., Marples, R. R. & Kligman, A. M. Staphylococcus aureus in the lesions of atopic dermatitis. Br. J. Dermatol. 90, 525–530 (1974).

    Article  CAS  PubMed  Google Scholar 

  90. Huang, J. T., Abrams, M., Tlougan, B., Rademaker, A. & Paller, A. S. Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics 123, e808–e814 (2009).

    Article  PubMed  Google Scholar 

  91. Aioi, A. et al. Impairment of skin barrier function in NC/Nga Tnd mice as a possible model for atopic dermatitis. Br. J. Dermatol. 144, 12–18 (2001).

    Article  CAS  PubMed  Google Scholar 

  92. Terada, M. et al. Contribution of IL-18 to atopic-dermatitis-like skin inflammation induced by Staphylococcus aureus product in mice. Proc. Natl Acad. Sci. USA 103, 8816–8821 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Frank, D. N. et al. Microbial diversity in chronic open wounds. Wound Repair Regen. 17, 163–172 (2009).

    Article  PubMed  Google Scholar 

  94. Dowd, S. E. et al. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol. 8, 43 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Smith, D. M. et al. Evaluation of the bacterial diversity of Pressure ulcers using bTEFAP pyrosequencing. BMC Med. Genomics 3, 41 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Price, L. B. et al. Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS ONE 4, e6462 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Polavarapu, N., Ogilvie, M. P. & Panthaki, Z. J. Microbiology of burn wound infections. J. Craniofac. Surg. 19, 899–902 (2008).

    Article  PubMed  Google Scholar 

  98. Grice, E. A. et al. Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defence response. Proc. Natl Acad. Sci. USA 107, 14799–14804 (2010). This study showed that a selective shift in microbiota is associated with an altered innate immune response.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Uckay, I. et al. Foreign body infections due to Staphylococcus epidermidis. Ann. Med. 41, 109–119 (2009).

    Article  CAS  PubMed  Google Scholar 

  100. Otto, M. Staphylococcus epidermidis — the 'accidental' pathogen. Nature Rev. Microbiol. 7, 555–567 (2009).

    Article  CAS  Google Scholar 

  101. Peterson, J. et al. The NIH Human Microbiome Project. Genome Res. 19, 2317–2323 (2009). A detailed description of the Human Microbiome Project and its objectives.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Iwase, T. et al. Staphylococcus epidermidis esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465, 346–349 (2010). An important paper demonstrating the mechanism by which S. epidermidis inhibits S. aureus colonization of the nare.

    Article  CAS  PubMed  Google Scholar 

  103. Dunbar, J., Barns, S. M., Ticknor, L. O. & Kuske, C. R. Empirical and theoretical bacterial diversity in four Arizona soils. Appl. Environ. Microbiol. 68, 3035–3045 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Bowler, P. G., Duerden, B. I. & Armstrong, D. G. Wound microbiology and associated approaches to wound management. Clin. Microbiol. Rev. 14, 244–269 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Davies, C. E. et al. Use of molecular techniques to study microbial diversity in the skin: chronic wounds reevaluated. Wound Repair Regen. 9, 332–340 (2001).

    Article  CAS  PubMed  Google Scholar 

  106. Hugenholtz, P. & Pace, N. R. Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol. 14, 190–197 (1996).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank H. Kong and E. Hobbs for critical reading of the manuscript and J. Fekecs and D. Leja for graphical assistance. E.A.G. is supported by a Pharmacology Research Associate Training Fellowship, US National Institute of General Medical Sciences. This work was supported by the US National Human Genome Research Institute Intramural Research Program and the US National Institutes of Health Common Fund AR057504.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia A. Segre.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Julia A. Segre's homepage

Glossary

Keratinocyte

The predominant cell type of the epidermis. Keratinocytes produce keratin as they terminally differentiate into the squames of the stratum corneum.

Squame

An enucleated, dead, squamous keratinocyte that is shed from the stratum corneum.

Sebum

The oily, lipid-containing substance that is secreted by the sebaceous glands of the skin. Sebaceous glands are connected to the hair follicle and form the pilosebaceous unit. Sebum protects and emolliates the skin and hair.

16S ribosomal RNA metagenomic sequencing

Genomic analysis of 16S ribosomal RNA phylotypes from DNA that is extracted directly from bacterial communities in clinical or environmental samples, a process that circumvents culturing.

Microbiome

All of the genetic material of a microbial community sequenced together.

Phylotype

A taxon-neutral way to describe organisms based on their phylogenetic relationships to other organisms. Phylotypes are determined by comparing 16S ribosomal RNA gene sequences. A common threshold used to define species-level phylotypes is 97% sequence identity of the 16S rRNA gene sequence.

Whole-genome shotgun metagenomic sequencing

Genomic analysis of DNA that is extracted directly from a clinical or environmental sample and whole-genome shotgun (WGS) sequenced to represent the full microbiome.

Pattern recognition receptor

(PRR). A receptor present on the surface of keratinocytes and other cells of the innate immune system that recognizes microorganism-specific molecules (for example, lipopolysaccharide and flagellin).

Pathogen-associated molecular pattern

(PAMP). A molecule that is associated with a pathogen and recognized by a pathogen recognition receptor. Examples include lipopolysaccharide, flagellin, lipoteichoic acid, double-stranded RNA, peptidoglycan and unmethylated CpG motifs.

Atopic dermatitis

(AD). A type of eczema characterized by red, flaky, itchy skin, typically affecting the inner elbows and behind the knees. It is often associated with other atopic diseases such as allergic rhinitis, hay fever and asthma

Seborrhoeic dermatitis

An inflammatory, hyperproliferative skin condition characterized by red, flaky, skin often affecting sebaceous areas of the face, scalp and trunk. Commonly known as dandruff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grice, E., Segre, J. The skin microbiome. Nat Rev Microbiol 9, 244–253 (2011). https://doi.org/10.1038/nrmicro2537

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2537

This article is cited by

Search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research