Abstract
As the largest organ of the human body, skin provides the first barrier against environmental insults, including invading pathogens. Many studies have defined commensal skin bacteria; more recent metagenomic studies have extended characterization of the microbiota to resident fungi and viruses. The skin is dominated by members of Actinobacteria, Firmicutes, Proteobacteria, Bacteroidetes, Malassezia spp., bacteriophages and human viruses. Defining the microbiota of both healthy and affected skin provides insight into the influence of the cutaneous microbiota on immune responses and disease states. Crosstalk between commensal microbiota and the innate immune system facilitates proper response and healing. Commensal bacteria appear to protect from pathogens directly by releasing antibacterial products and indirectly by stimulating innate immune responses. Skin pathologies such as atopic dermatitis, rosacea, psoriasis and acne are characterized by disruptions of certain immune pathways and imbalances of skin microbiota. Additionally, susceptibility to skin infection appears to be influenced by the microbial community present on the skin, while infection and the resultant immune response alters the skin microbiota. Understanding the role of the skin microbiota in skin disorders and infection may lead to novel therapies that aim to restore the balance of commensal skin microbes.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC (2012) Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 129:434–440, 440 e431–e432
Alekseyenko AV, Perez-Perez GI, De Souza A, Strober B, Gao Z, Bihan M, Li K, Methe BA, Blaser MJ (2013) Community differentiation of the cutaneous microbiota in psoriasis. Microbiome 1:31
Ayer J, Burrows N (2006) Acne: more than skin deep. Postgrad Med J 82:500–506
Bek-Thomsen M, Lomholt HB, Kilian M (2008) Acne is not associated with yet-uncultured bacteria. J Clin Microbiol 46:3355–3360
Berg M, Liden S (1989) An epidemiological study of rosacea. Acta Derm Venereol 69:419–423
Blaser MJ, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Estrada I, Gao Z, Clemente JC, Costello EK, Knight R (2013) Distinct cutaneous bacterial assemblages in a sampling of South American Amerindians and US residents. ISME J 7:85–95
Capone KA, Dowd SE, Stamatas GN, Nikolovski J (2011) Diversity of the human skin microbiome early in life. J Invest Dermatol 131:2026–2032
Casas C, Paul C, Lahfa M, Livideanu B, Lejeune O, Alvarez-Georges S, Saint-Martory C, Degouy A, Mengeaud V, Ginisty H, Durbise E, Schmitt AM, Redoules D (2012) Quantification of Demodex folliculorum by PCR in rosacea and its relationship to skin innate immune activation. Exp Dermatol 21:906–910
Chehoud C, Rafail S, Tyldsley AS, Seykora JT, Lambris JD, Grice EA (2013) Complement modulates the cutaneous microbiome and inflammatory milieu. Proc Natl Acad Sci USA 110:15061–15066
Christophers E (2001) Psoriasis—epidemiology and clinical spectrum. Clin Exp Dermatol 26:314–320
Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z, Wang B, Magris M, Hidalgo G, Contreras M, Noya-Alarcon O, Lander O, McDonald J, Cox M, Walter J, Oh PL, Ruiz JF, Rodriguez S, Shen N, Song SJ, Metcalf J, Knight R, Dantas G, Dominguez-Bello MG (2015) The microbiome of uncontacted Amerindians. Sci Adv 1:e1500183
Cogen AL, Yamasaki K, Sanchez KM, Dorschner RA, Lai Y, MacLeod DT, Torpey JW, Otto M, Nizet V, Kim JE, Gallo RL (2010) 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
Cogen AL, Walker SL, Roberts CH, Hagge DA, Neupane KD, Khadge S, Lockwood DN (2012) Human beta-defensin 3 is up-regulated in cutaneous leprosy type 1 reactions. PLoS Negl Trop Dis 6:e1869
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697
Crawford GH, Pelle MT, James WD (2004) Rosacea: I. Etiology, pathogenesis, and subtype classification. J Am Acad Dermatol 51:327–341; quiz 342–344
Dahl MV, Ross AJ, Schlievert PM (2004) Temperature regulates bacterial protein production: possible role in rosacea. J Am Acad Dermatol 50:266–272
Decreau RA, Marson CM, Smith KE, Behan JM (2003) 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
Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) 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
Drake DR, Brogden KA, Dawson DV, Wertz PW (2008) Thematic review series: skin lipids. Antimicrobial lipids at the skin surface. J Lipid Res 49:4–11
Elias PM (2007) The skin barrier as an innate immune element. Semin Immunopathol 29:3–14
Fahlen A, Engstrand L, Baker BS, Powles A, Fry L (2012) Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res 304:15–22
Fernandez-Obregon A, Patton DL (2007) The role of Chlamydia pneumoniae in the etiology of acne rosacea: response to the use of oral azithromycin. Cutis 79:163–167
Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105:17994–17999
Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, Schoenfeld D, Nomicos E, Park M, Program NIHISCCS, Kong HH, Segre JA (2013) Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367–370
Fitz-Gibbon S, Tomida S, Chiu BH, Nguyen L, Du C, Liu M, Elashoff D, Erfe MC, Loncaric A, Kim J, Modlin RL, Miller JF, Sodergren E, Craft N, Weinstock GM, Li H (2013) Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol 133:2152–2160
Foolad N, Brezinski EA, Chase EP, Armstrong AW (2013) Effect of nutrient supplementation on atopic dermatitis in children: a systematic review of probiotics, prebiotics, formula, and fatty acids. JAMA Dermatol 149:350–355
Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, Pariente K, Segondy M, Burguiere A, Manuguerra JC, Caro V, Eloit M (2012) Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS ONE 7:e38499
Fry L, Baker BS, Powles AV, Fahlen A, Engstrand L (2013) Is chronic plaque psoriasis triggered by microbiota in the skin? Br J Dermatol 169:47–52
Fuchs-Tarlovsky V, Marquez-Barba MF, Sriram K (2015) Probiotics in dermatologic practice. Nutrition 32:289–295
Gallo RL, Nakatsuji T (2011) Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol 131:1974–1980
Gao Z, Tseng CH, Pei Z, Blaser MJ (2007) Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 104:2927–2932
Gao Z, Tseng CH, Strober BE, Pei Z, Blaser MJ (2008) Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE 3:e2719
Ghinai R, El-Duah P, Chi KH, Pillay A, Solomon AW, Bailey RL, Agana N, Mabey DC, Chen CY, Adu-Sarkodie Y, Marks M (2015) A cross-sectional study of ‘yaws’ in districts of ghana which have previously undertaken azithromycin mass drug administration for trachoma control. PLoS Negl Trop Dis 9:e0003496
Grice EA (2014) The skin microbiome: potential for novel diagnostic and therapeutic approaches to cutaneous disease. Semin Cutan Med Surg 33:98–103
Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253
Grice EA, Kong HH, Renaud G, Young AC, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050
Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Program NCS, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192
Grice EA, Snitkin ES, Yockey LJ, Bermudez DM, Program NCS, Liechty KW, Segre JA (2010) Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. Proc Natl Acad Sci USA 107:14799–14804
Hannigan GD, Meisel JS, Tyldsley AS, Zheng Q, Hodkinson BP, SanMiguel AJ, Minot S, Bushman FD, Grice EA (2015) The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. MBio 6:e01578-15
Holmes AD (2013) Potential role of microorganisms in the pathogenesis of rosacea. J Am Acad Dermatol 69:1025–1032
Horton JM, Gao Z, Sullivan DM, Shopsin B, Perez-Perez GI, Blaser MJ (2015) The cutaneous microbiome in outpatients presenting with acute skin abscesses. J Infect Dis 211:1895–1904
Huang JT, Abrams M, Tlougan B, Rademaker A, Paller AS (2009) Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics 123:e808–e814
Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–349
Janowicz DM, Ofner S, Katz BP, Spinola SM (2009) Experimental infection of human volunteers with Haemophilus ducreyi: fifteen years of clinical data and experience. J Infect Dis 199:1671–1679
Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Program NCS, Murray PR, Turner ML, Segre JA (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859
Lacey N, Delaney S, Kavanagh K, Powell FC (2007) Mite-related bacterial antigens stimulate inflammatory cells in rosacea. Br J Dermatol 157:474–481
Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, Wu ZR, Hooper LV, Schmidt RR, von Aulock S, Radek KA, Huang CM, Ryan AF, Gallo RL (2009) Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 15:1377–1382
Lai Y, Cogen AL, Radek KA, Park HJ, Macleod DT, Leichtle A, Ryan AF, Di Nardo A, Gallo RL (2010) Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol 130:2211–2221
Leung DY, Travers JB, Giorno R, Norris DA, Skinner R, Aelion J, Kazemi LV, Kim MH, Trumble AE, Kotb M et al (1995) Evidence for a streptococcal superantigen-driven process in acute guttate psoriasis. J Clin Invest 96:2106–2112
Leyden JJ, Del Rosso JQ (2011) Oral antibiotic therapy for acne vulgaris: pharmacokinetic and pharmacodynamic perspectives. J Clin Aesthetic Dermatol 4:40–47
Leyden JJ, McGinley KJ, Mills OH, Kligman AM (1975) Propionibacterium levels in patients with and without acne vulgaris. J Invest Dermatol 65:382–384
Marks M, Chi KH, Vahi V, Pillay A, Sokana O, Pavluck A, Mabey DC, Chen CY, Solomon AW (2014) Haemophilus ducreyi associated with skin ulcers among children, Solomon Islands. Emerg Infect Dis 20:1705–1707
Meisel JS, Hannigan GD, Tyldsley AS, SanMiguel AJ, Hodkinson BP, Zheng Q, Grice EA (2016) Skin microbiome surveys are strongly influenced by experimental design. J Invest Dermatol 136:947–956
Mitjà O, Lukehart SA, Pokowas G, Moses P, Kapa A, Godornes C, Robson J, Cherian S, Houinei W, Kazadi W, Siba P, de Lazzari E, Bassat Q (2014) Haemophilus ducreyi as a cause of skin ulcers in children from a yaws-endemic area of Papua New Guinea: a prospective cohort study. Lancet Glob Health 2:e235–e241
Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, Talan DA, Group EMINS (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355:666–674
Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R, Kastenmuller W, Deming C, Quinones M, Koo L, Conlan S, Spencer S, Hall JA, Dzutsev A, Kong H, Campbell DJ, Trinchieri G, Segre JA, Belkaid Y (2012) Compartmentalized control of skin immunity by resident commensals. Science 337:1115–1119
Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL (2013) The microbiome extends to subepidermal compartments of normal skin. Nat Commun 4:1431
Numata S, Akamatsu H, Akaza N, Yagami A, Nakata S, Matsunaga K (2014) Analysis of facial skin-resident microbiota in Japanese acne patients. Dermatology 228:86–92
Oh J, Conlan S, Polley EC, Segre JA, Kong HH (2012) Shifts in human skin and nares microbiota of healthy children and adults. Genome Med 4:77
Oh J, Freeman AF, Program NCS, Park M, Sokolic R, Candotti F, Holland SM, Segre JA, Kong HH (2013) The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Genome Res 23:2103–2114
Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, Segre JA (2014) Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64
Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR Jr, Hendrix RW, Hatfull GF (2003) Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182
Picardo M, Ottaviani M (2014) Skin microbiome and skin disease: the example of rosacea. J Clin Gastroenterol 48(Suppl 1):S85–S86
Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87
Scholz F, Badgley BD, Sadowsky MJ, Kaplan DH (2014) Immune mediated shaping of microflora community composition depends on barrier site. PLoS ONE 9:e84019
Smeekens SP, Huttenhower C, Riza A, van de Veerdonk FL, Zeeuwen PL, Schalkwijk J, van der Meer JW, Xavier RJ, Netea MG, Gevers D (2014) Skin microbiome imbalance in patients with STAT1/STAT3 defects impairs innate host defense responses. J Innate Immun 6:253–262
Staudinger T, Pipal A, Redl B (2011) Molecular analysis of the prevalent microbiota of human male and female forehead skin compared to forearm skin and the influence of make-up. J Appl Microbiol 110:1381–1389
Toshkova K, Annemuller C, Akineden O, Lammler C (2001) The significance of nasal carriage of Staphylococcus aureus as risk factor for human skin infections. FEMS Microbiol Lett 202:17–24
Tuzun Y, Keskin S, Kote E (2010) The role of Helicobacter pylori infection in skin diseases: facts and controversies. Clin Dermatol 28:478–482
Uehara Y, Nakama H, Agematsu K, Uchida M, Kawakami Y, Abdul Fattah AS, Maruchi N (2000) Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect 44:127–133
van Rensburg JJ, Lin H, Gao X, Toh E, Fortney KR, Ellinger S, Zwickl B, Janowicz DM, Katz BP, Nelson DE, Dong Q, Spinola SM (2015) The human skin microbiome associates with the outcome of and is influenced by bacterial infection. MBio 6:e01315-15
Wang Y, Kuo S, Shu M, Yu J, Huang S, Dai A, Two A, Gallo RL, Huang CM (2014) Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Appl Microbiol Biotechnol 98:411–424
Yamasaki K, Di Nardo A, Bardan A, Murakami M, Ohtake T, Coda A, Dorschner RA, Bonnart C, Descargues P, Hovnanian A, Morhenn VB, Gallo RL (2007) Increased serine protease activity and cathelicidin promotes skin inflammation in rosacea. Nat Med 13:975–980
Yamasaki K, Kanada K, Macleod DT, Borkowski AW, Morizane S, Nakatsuji T, Cogen AL, Gallo RL (2011) TLR2 expression is increased in rosacea and stimulates enhanced serine protease production by keratinocytes. J Invest Dermatol 131:688–697
Zeeuwen PL, Boekhorst J, van den Bogaard EH, de Koning HD, van de Kerkhof PM, Saulnier DM, van Swam II, van Hijum SA, Kleerebezem M, Schalkwijk J, Timmerman HM (2012) Microbiome dynamics of human epidermis following skin barrier disruption. Genome Biol 13:R101
Acknowledgments
We thank David Nelson for critical reading of this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
van Rensburg, J.J., Dbeibo, L., Spinola, S.M. (2016). The Cutaneous Microbiota as a Determinant of Skin Barrier Function: Molecular Interactions and Therapeutic Opportunities. In: Wondrak, G. (eds) Skin Stress Response Pathways. Springer, Cham. https://doi.org/10.1007/978-3-319-43157-4_18
Download citation
DOI: https://doi.org/10.1007/978-3-319-43157-4_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-43155-0
Online ISBN: 978-3-319-43157-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)