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The Microbiota of the Human Skin

  • Markus EgertEmail author
  • Rainer Simmering
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 902)

Abstract

The aim of this chapter is to sum up important progress in the field of human skin microbiota research that was achieved over the last years.

The human skin is one of the largest and most versatile organs of the human body. Owing to its function as a protective interface between the largely sterile interior of the human body and the highly microbially contaminated outer environment, it is densely colonized with a diverse and active microbiota. This skin microbiota is of high importance for human health and well-being. It is implicated in several severe skin diseases and plays a major role in wound infections. Many less severe, but negatively perceived cosmetic skin phenomena are linked with skin microbes, too. In addition, skin microorganisms, in particular on the human hands, are crucial for the field of hygiene research. Notably, apart from being only a potential source of disease and contamination, the skin microbiota also contributes to the protective functions of the human skin in many ways. Finally, the analysis of structure and function of the human skin microbiota is interesting from a basic, evolutionary perspective on human microbe interactions.

Key questions in the field of skin microbiota research deal with (a) a deeper understanding of the structure (species inventory) and function (physiology) of the healthy human skin microbiota in space and time, (b) the distinction of resident and transient skin microbiota members, (c) the distinction of beneficial skin microorganisms from microorganisms or communities with an adverse or sickening effect on their hosts, (d) factors shaping the skin microbiota and its functional role in health and disease, (e) strategies to manipulate the skin microbiota for therapeutic reasons.

Keywords

Skin microbiota Bacteria Archaea Fungi Actinobacteria Firmicutes Proteobacteria Homeostasis Skin diseases Skin defense and immunity Cosmetics Perspiration 

References

  1. Akiyama H, Yamasaki O, Tada J, Arata J (2000) Adherence characteristics and susceptibility to antimicrobial agents of Staphylococcus aureus strains isolated from skin infections and atopic dermatitis. J Dermatol Sci 23:155–160PubMedCrossRefGoogle Scholar
  2. Alekseyenko AV, Perez-Perez GI, De Souza A, Strober B, Gao Z, Bihan M, Li K, Methé BA, Blaser MJ (2013) Community differentiation of the cutaneous microbiota in psoriasis. Microbiome 1:31. doi: 10.1186/2049-2618-1-31 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Al-Ghazzewi FH, Tester RF (2014) Impact of prebiotics and probiotics on skin health. Benefic Microbes 5:99–107. doi: 10.3920/BM2013.0040 CrossRefGoogle Scholar
  4. Bawdon D, Cox DS, Ashford D, James AG, Thomas GH (2015) Identification of axillary Staphylococcus sp. involved in the production of the malodorous thioalcohol 3-methyl-3-sufanylhexan-1-ol. FEMS Microbiol Lett 362:fnv111. doi: 10.1093/femsle/fnv111 PubMedCrossRefGoogle Scholar
  5. Bek-Thomsen M, Lomholt HB, Kilian M (2008) Acne is not associated with yet-uncultured bacteria. J Clin Microbiol 46:3355–3360. doi: 10.1128/JCM.00799-08 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Belkaid Y, Naik S (2013) Compartmentalized and systemic control of tissue immunity by commensals. Nat Immunol 14:646–653. doi: 10.1038/ni.2604 PubMedCrossRefGoogle Scholar
  7. Belkaid Y, Segre JA (2014) Dialogue between skin microbiota and immunity. Science 346:954–959. doi: 10.1126/science.1260144 PubMedCrossRefGoogle Scholar
  8. Bockmühl DP (2004) Präbiotika für kosmetische Anwendungen. SÖFW J 130:3–6Google Scholar
  9. Bockmühl DP, Jassoy C, Nieveler S, Scholtyssek R, Wadle A, Waldmann-Laue M (2006) Prebiotic cosmetics: an alternative to antibacterial products. IFSCC Mag 9:197–200Google Scholar
  10. Bojar, Holland (2002) Review: the human cutaneous microflora and factors controlling colonisation. World J Microbiol Biotechnol 18:889–903. doi: 10.1023/A:1021271028979 CrossRefGoogle Scholar
  11. Braff MH, Gallo RL (2006) Antimicrobial peptides: an essential component of the skin defensive barrier. Curr Top Microbiol Immunol 306:91–110PubMedGoogle Scholar
  12. Braff MH, Bardan A, Nizet V, Gallo RL (2005) Cutaneous defense mechanisms by antimicrobial peptides. J Invest Dermatol 125:9–13. doi: 10.1111/j.0022-202X.2004.23587.x PubMedCrossRefGoogle Scholar
  13. Brüggemann H (2005) Insights in the pathogenic potential of Propionibacterium acnes from its complete genome. Semin Cutan Med Surg 24:67–72. doi: 10.1016/j.sder.2005.03.001 PubMedCrossRefGoogle Scholar
  14. Brüggemann H, Henne A, Hoster F, Liesegang H, Wiezer A, Strittmatter A, Hujer S, Dürre P, Gottschalk G (2004) The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305:671–673. doi: 10.1126/science.1100330 PubMedCrossRefGoogle Scholar
  15. Callewaert C, Hutapea P, Van de Wiele T, Boon N (2014) Deodorants and antiperspirants affect the axillary bacterial community. Arch Dermatol Res. doi: 10.1007/s00403-014-1487-1 PubMedGoogle Scholar
  16. Canesso MCC, Vieira AT, Castro TBR, Schirmer BGA, Cisalpino D, Martins FS, Rachid MA, Nicoli JR, Teixeira MM, Barcelos LS (2014) Skin wound healing is accelerated and scarless in the absence of commensal microbiota. J Immunol 193:5171–5180. doi: 10.4049/jimmunol.1400625 PubMedCrossRefGoogle Scholar
  17. Capone KA, Dowd SE, Stamatas GN, Nikolovski J (2011) Diversity of the human skin microbiome early in life. J Investig Dermatol 131:2026–2032. doi: 10.1038/jid.2011.168 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Carolan H, Watkins S, Bradshaw D (2008) The prebiotic concept-a novel aproach for skin health. Euro Cosmet 7(8):22–27Google Scholar
  19. Christensen GJM, Brüggemann H (2014) Bacterial skin commensals and their role as host guardians. Benefic Microbes 5:201–215. doi: 10.3920/BM2012.0062 CrossRefGoogle Scholar
  20. Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z, Wang B, Magris M, Hidalgo G, Contreras M, Noya-Alarcón Ó, 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. doi: 10.1126/sciadv.1500183 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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. doi: 10.1038/jid.2009.243 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cosseau C, Devine DA, Dullaghan E, Gardy JL, Chikatamarla A, Gellatly S, Yu LL, Pistolic J, Falsafi R, Tagg J, Hancock REW (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76:4163–4175. doi: 10.1128/IAI.00188-08 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dethlefsen L, Relman DA (2011) Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A 108(Suppl 1):4554–4561. doi: 10.1073/pnas.1000087107 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 107:11971–11975. doi: 10.1073/pnas.1002601107 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Donnarumma G, Paoletti I, Buommino E, Orlando M, Tufano MA, Baroni A (2004) Malassezia furfur induces the expression of beta-defensin-2 in human keratinocytes in a protein kinase C-dependent manner. Arch Dermatol Res 295:474–481. doi: 10.1007/s00403-003-0445-0 PubMedCrossRefGoogle Scholar
  26. Edmonds-Wilson SL, Nurinova NI, Zapka CA, Fierer N, Wilson M (2015) Review of human hand microbiome research. J Dermatol Sci. doi: 10.1016/j.jdermsci.2015.07.006 PubMedGoogle Scholar
  27. Egert M, Schmidt I, Höhne H-M, Lachnit T, Schmitz RA, Breves R (2011) rRNA-based profiling of bacteria in the axilla of healthy males suggests right-left asymmetry in bacterial activity. FEMS Microbiol Ecol 77:146–153. doi: 10.1111/j.1574-6941.2011.01097.x PubMedCrossRefGoogle Scholar
  28. Egert M, Höhne H-M, Weber T, Simmering R, Banowski B, Breves R (2013) Identification of compounds inhibiting the C-S lyase activity of a cell extract from a Staphylococcus sp. isolated from human skin. Lett Appl Microbiol 57:534–539. doi: 10.1111/lam.12146 PubMedCrossRefGoogle Scholar
  29. Egert M, Simmering R, Banowski B, Breves R (2014) In Deo veritas—Entstehung und Verhinderung humanen Körpergeruchs. BIOspektrum 20:497–499. doi: 10.1007/s12268-014-0469-3 CrossRefGoogle Scholar
  30. 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 105:17994–17999. doi: 10.1073/pnas.0807920105 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, Schoenfeld D, Nomicos E, Park M, Becker J, Benjamin B, Blakesley R, Bouffard G, Brooks S, Coleman H, Dekhtyar M, Gregory M, Guan X, Gupta J, Han J, Hargrove A, Ho S, Johnson T, Legaspi R, Lovett S, Maduro Q, Masiello C, Maskeri B, McDowell J, Montemayor C, Mullikin J, Park M, Riebow N, Schandler K, Schmidt B, Sison C, Stantripop M, Thomas J, Thomas P, Vemulapalli M, Young A, Kong HH, Segre JA (2013) Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367–370. doi: 10.1038/nature12171 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Finlay BB, Hancock REW (2004) Can innate immunity be enhanced to treat microbial infections? Nat Rev Microbiol 2:497–504. doi: 10.1038/nrmicro908 PubMedCrossRefGoogle Scholar
  33. Forney L, Zhou X, Brown C (2004) Molecular microbial ecology: land of the one-eyed king. Curr Opin Microbiol 7:210–220. doi: 10.1016/j.mib.2004.04.015 PubMedCrossRefGoogle Scholar
  34. Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, Pariente K, Segondy M, Burguière A, Manuguerra J-C, 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. doi: 10.1371/journal.pone.0038499 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fredrich E, Barzantny H, Brune I, Tauch A (2013) Daily battle against body odor: towards the activity of the axillary microbiota. Trends Microbiol 21:305–312. doi: 10.1016/j.tim.2013.03.002 PubMedCrossRefGoogle Scholar
  36. Frohm M, Agerberth B, Ahangari G, Stâhle-Bäckdahl M, Lidén S, Wigzell H, Gudmundsson GH (1997) The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratinocytes during inflammatory disorders. J Biol Chem 272:15258–15263PubMedCrossRefGoogle Scholar
  37. Fujii T, Shinozaki J, Kajiura T, Iwasaki K, Fudou R (2014) A newly discovered Anaerococcus strain responsible for axillary odor and a new axillary odor inhibitor, pentagalloyl glucose. FEMS Microbiol Ecol 89:198–207. doi: 10.1111/1574-6941.12347 PubMedCrossRefGoogle Scholar
  38. Gao Z, Tseng C, Pei Z, Blaser MJ (2007) Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci U S A 104:2927–2932. doi: 10.1073/pnas.0607077104 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gao Z, Tseng C, Strober BE, Pei Z, Blaser MJ (2008) Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE 3:e2719. doi: 10.1371/journal.pone.0002719 PubMedPubMedCentralCrossRefGoogle Scholar
  40. García JR, Krause A, Schulz S, Rodríguez-Jiménez FJ, Klüver E, Adermann K, Forssmann U, Frimpong-Boateng A, Bals R, Forssmann WG (2001) Human beta-defensin 4: a novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J 15:1819–1821PubMedGoogle Scholar
  41. Giacomoni PU, Mammone T, Teri M (2009) Gender-linked differences in human skin. J Dermatol Sci 55:144–149. doi: 10.1016/j.jdermsci.2009.06.001 PubMedCrossRefGoogle Scholar
  42. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412PubMedGoogle Scholar
  43. Grice EA (2014) The skin microbiome: potential for novel diagnostic and therapeutic approaches to cutaneous disease. Semin Cutan Med Surg 33:98–103PubMedPubMedCentralCrossRefGoogle Scholar
  44. Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253. doi: 10.1038/nrmicro2537 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Comparative Sequencing Program NISC, 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. doi: 10.1126/science.1171700 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hannigan GD, Hodkinson BP, McGinnis K, Tyldsley AS, Anari JB, Horan AD, Grice EA, Mehta S (2014) Culture-independent pilot study of microbiota colonizing open fractures and association with severity, mechanism, location, and complication from presentation to early outpatient follow-up. J Orthop Res 32:597–605. doi: 10.1002/jor.22578 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Harder J, Schroder J-M (2002) RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J Biol Chem 277:46779–46784. doi: 10.1074/jbc.M207587200 PubMedCrossRefGoogle Scholar
  48. Harder J, Bartels J, Christophers E, Schroder JM (2001) Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276:5707–5713. doi: 10.1074/jbc.M008557200 PubMedCrossRefGoogle Scholar
  49. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, Minbiole KPC (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3:818–824. doi: 10.1038/ismej.2009.27 PubMedCrossRefGoogle Scholar
  50. Horz H-P (2015) Archaeal lineages within the human microbiome: absent, rare or elusive? Life (Basel) 5:1333–1345. doi: 10.3390/life5021333 Google Scholar
  51. Horz H-P, Conrads G (2010) The discussion goes on: what is the role of euryarchaeota in humans? Archaea 2010:1–8. doi: 10.1155/2010/967271 CrossRefGoogle Scholar
  52. Hulcr J, Latimer AM, Henley JB, Rountree NR, Fierer N, Lucky A, Lowman MD, Dunn RR (2012) A jungle in there: bacteria in belly buttons are highly diverse, but predictable. PLoS ONE 7:e47712. doi: 10.1371/journal.pone.0047712 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Iovieno A, Lambiase A, Sacchetti M, Stampachiacchiere B, Micera A, Bonini S (2008) Preliminary evidence of the efficacy of probiotic eye-drop treatment in patients with vernal keratoconjunctivitis. Graefes Arch Clin Exp Ophthalmol 246:435–441. doi: 10.1007/s00417-007-0682-6 PubMedCrossRefGoogle Scholar
  54. 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. doi: 10.1038/nature09074 PubMedCrossRefGoogle Scholar
  55. James AG, Austin CJ, Cox DS, Taylor D, Calvert R (2013) Microbiological and biochemical origins of human axillary odour. FEMS Microbiol Ecol 83:527–540. doi: 10.1111/1574-6941.12054 PubMedCrossRefGoogle Scholar
  56. Janssen F, Waldmann-Laue M (2008) Efficacy of a prebiotic product combination against skin impurities. Presented at the IFSCC Conference, BarcelonaGoogle Scholar
  57. Julian TR, Leckie JO, Boehm AB (2010) Virus transfer between fingerpads and fomites: virus transfer between fingerpads and fomites. J Appl Microbiol 109:1868–1874. doi: 10.1111/j.1365-2672.2010.04814.x PubMedCrossRefGoogle Scholar
  58. Katsuyama M, Wachi Y, Ikezawa Z, Kitamura K, Suga C, Ohnuma S (1997) Correlation between the population of Staphylococcus aureus on the skin and severity of a score of dry type atopic dermatitis conditions. Nippon Hifuka Gakkai Zasshi 107:1103–1111Google Scholar
  59. Katsuyama M, Masako K, Kobayashi Y, Yusuke K, Ichikawa H, Hideyuki I, Mizuno A, Atsuko M, Miyachi Y, Yoshiki M, Matsunaga K, Kayoko M, Kawashima M, Makoto K (2005) A novel method to control the balance of skin microflora Part 2. A study to assess the effect of a cream containing farnesol and xylitol on atopic dry skin. J Dermatol Sci 38:207–213. doi: 10.1016/j.jdermsci.2005.01.003 PubMedCrossRefGoogle Scholar
  60. Kelly DP, Wood AP (2010) Skin microbiology, body odor, and methylotrophic bacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology., Biomedical and life sciences. Springer, Heidelberg, pp 3203–3213Google Scholar
  61. Kimoto-Nira H, Aoki R, Sasaki K, Suzuki C, Mizumachi K (2012) Oral intake of heat-killed cells of Lactococcus lactis strain H61 promotes skin health in women. J Nutr Sci 1:e18. doi: 10.1017/jns.2012.22 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kong HH (2011) Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328. doi: 10.1016/j.molmed.2011.01.013 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kong HH, Segre JA (2012) Skin microbiome: looking back to move forward. J Investig Dermatol 132:933–939. doi: 10.1038/jid.2011.417 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Comparative Sequence Program NISC, 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. doi: 10.1101/gr.131029.111 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kozuka T (2002) Patch testing to exclude allergic contact dermatitis caused by povidone-iodine. Dermatol (Basel) 204(Suppl 1):96–98, doi:57734CrossRefGoogle Scholar
  66. Krutmann J (2009) Pre- and probiotics for human skin. J Dermatol Sci 54:1–5. doi: 10.1016/j.jdermsci.2009.01.002 PubMedCrossRefGoogle Scholar
  67. Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, Cogen AL, Wu Z-R, Hooper LV, Schmidt RR, von Aulock S, Radek KA, Huang C-M, Ryan AF, Gallo RL (2009) Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 15:1377–1382. doi: 10.1038/nm.2062 PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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. doi: 10.1038/jid.2010.123 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lang C, Heilmann A, Veen M, Budde E, Böttner M, Reindl A, Knöll R (2006) Methods and means for protecting the skin against pathogenic bacteria. U.S. patent WO 2006/136420 A2Google Scholar
  70. Mao G-Y, Yang S-L, Zheng J-H (2008) Etiology and management of axillary bromidrosis: a brief review. Int J Dermatol 47:1063–1068. doi: 10.1111/j.1365-4632.2008.03735.x PubMedCrossRefGoogle Scholar
  71. McAleer MA, Irvine AD (2013) The multifunctional role of filaggrin in allergic skin disease. J Allergy Clin Immunol 131:280–291. doi: 10.1016/j.jaci.2012.12.668 PubMedCrossRefGoogle Scholar
  72. Meadow JF, Bateman AC, Herkert KM, O’Connor TK, Green JL (2013) Significant changes in the skin microbiome mediated by the sport of roller derby. Peer J 1:e53. doi: 10.7717/peerj.53 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Midorikawa K, Ouhara K, Komatsuzawa H, Kawai T, Yamada S, Fujiwara T, Yamazaki K, Sayama K, Taubman MA, Kurihara H, Hashimoto K, Sugai M (2003) Staphylococcus aureus susceptibility to innate antimicrobial peptides, beta-defensins and CAP18, expressed by human keratinocytes. Infect Immun 71:3730–3739PubMedPubMedCentralCrossRefGoogle Scholar
  74. Min YW, Rhee P-L (2015) The role of microbiota on the gut immunology. Clin Ther 37:968–975. doi: 10.1016/j.clinthera.2015.03.009 PubMedCrossRefGoogle Scholar
  75. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD (2011) The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21:1616–1625. doi: 10.1101/gr.122705.111 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Invest 124:4212–4218. doi: 10.1172/JCI72333 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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. doi: 10.1126/science.1225152 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nakamizo S, Egawa G, Honda T, Nakajima S, Belkaid Y, Kabashima K (2015) Commensal bacteria and cutaneous immunity. Semin Immunopathol 37:73–80. doi: 10.1007/s00281-014-0452-6 PubMedCrossRefGoogle Scholar
  79. Nakatsuji T, Chiang H-I, Jiang SB, Nagarajan H, Zengler K, Gallo RL (2013) The microbiome extends to subepidermal compartments of normal skin. Nat Commun 4:1431. doi: 10.1038/ncomms2441 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Noël F, Piérard-Franchimont C, Piérard GE, Quatresooz P (2012) Sweaty skin, background and assessments. Int J Dermatol 51:647–655. doi: 10.1111/j.1365-4632.2011.05307.x PubMedCrossRefGoogle Scholar
  81. Nomura I, Gao B, Boguniewicz M, Darst MA, Travers JB, Leung DY m (2003) 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. doi: 10.1016/j.jaci.2003.08.049 PubMedCrossRefGoogle Scholar
  82. Ogawa T, Katsuoka K, Kawano K, Nishiyama S (1994) Comparative study of staphylococcal flora on the skin surface of atopic dermatitis patients and healthy subjects. J Dermatol 21:453–460PubMedCrossRefGoogle Scholar
  83. Oh J, Freeman AF, Comparative Sequencing Program NISC, 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. doi: 10.1101/gr.159467.113 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DYM (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347:1151–1160. doi: 10.1056/NEJMoa021481 PubMedCrossRefGoogle Scholar
  85. Ouwehand AC, Båtsman A, Salminen S (2003) Probiotics for the skin: a new area of potential application? Lett Appl Microbiol 36:327–331PubMedCrossRefGoogle Scholar
  86. Park HK, Ha M-H, Park S-G, Kim MN, Kim BJ, Kim W (2012) Characterization of the fungal microbiota (mycobiome) in healthy and dandruff-afflicted human scalps. PLoS ONE 7:e32847. doi: 10.1371/journal.pone.0032847 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Percival SL, Emanuel C, Cutting KF, Williams DW (2012) Microbiology of the skin and the role of biofilms in infection. Int Wound J 9:14–32. doi: 10.1111/j.1742-481X.2011.00836.x PubMedCrossRefGoogle Scholar
  88. Pernet I, Reymermier C, Guezennec A, Viac J, Guesnet J, Perrier E (2005) An optimized method for intensive screening of molecules that stimulate beta-defensin 2 or 3 (hBD2 or hBD3) expression in cultured normal human keratinocytes. Int J Cosmet Sci 27:161–170. doi: 10.1111/j.1467-2494.2005.00262.x PubMedCrossRefGoogle Scholar
  89. Philpott MP (2003) Defensins and acne. Mol Immunol 40:457–462PubMedCrossRefGoogle Scholar
  90. Picardo M, Ottaviani M (2014) Skin microbiome and skin disease: the example of rosacea. J Clin Gastroenterol 48(Suppl 1):S85–S86. doi: 10.1097/MCG.0000000000000241 PubMedCrossRefGoogle Scholar
  91. Probst AJ, Auerbach AK, Moissl-Eichinger C (2013) Archaea on human skin. PLoS ONE 8:e65388. doi: 10.1371/journal.pone.0065388 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Redel H, Gao Z, Li H, Alekseyenko AV, Zhou Y, Perez-Perez GI, Weinstock G, Sodergren E, Blaser MJ (2013) Quantitation and composition of cutaneous microbiota in diabetic and nondiabetic men. J Infect Dis 207:1105–1114. doi: 10.1093/infdis/jit005 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Rosenthal M, Goldberg D, Aiello A, Larson E, Foxman B (2011) Skin microbiota: microbial community structure and its potential association with health and disease. Infect Genet Evol 11:839–848. doi: 10.1016/j.meegid.2011.03.022 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Roth RR, James WD (1988) Microbial ecology of the skin. Annu Rev Microbiol 42:441–464. doi: 10.1146/annurev.mi.42.100188.002301 PubMedCrossRefGoogle Scholar
  95. Sanford JA, Gallo RL (2013) Functions of the skin microbiota in health and disease. Semin Immunol 25:370–377. doi: 10.1016/j.smim.2013.09.005 PubMedPubMedCentralCrossRefGoogle Scholar
  96. SanMiguel A, Grice EA (2015) Interactions between host factors and the skin microbiome. Cell Mol Life Sci 72:1499–1515. doi: 10.1007/s00018-014-1812-z PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sato K, Kang WH, Saga K, Sato KT (1989) Biology of sweat glands and their disorders. I. Normal sweat gland function. J Am Acad Dermatol 20:537–563PubMedCrossRefGoogle Scholar
  98. Scharschmidt TC, Fischbach MA (2013) What lives on our skin: ecology. Genomics and therapeutic opportunities of the skin microbiome. Drug Discov Today Dis Mech 10:e83–e89. doi: 10.1016/j.ddmec.2012.12.003 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Schauber J, Gallo RL (2008) Antimicrobial peptides and the skin immune defense system. J Allergy Clin Immunol 122:261–266. doi: 10.1016/j.jaci.2008.03.027 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Schommer NN, Gallo RL (2013) Structure and function of the human skin microbiome. Trends Microbiol 21:660–668. doi: 10.1016/j.tim.2013.10.001 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Seite S, Flores GE, Henley JB, Martin R, Zelenkova H, Aguilar L, Fierer N (2014) Microbiome of affected and unaffected skin of patients with atopic dermatitis before and after emollient treatment. J Drugs Dermatol 13:1365–1372PubMedGoogle Scholar
  102. Simmering R, Breves R (2009) Pre- and probiotic cosmetics. Hautarzt 60:809–814. doi: 10.1007/s00105-009-1759-4 PubMedCrossRefGoogle Scholar
  103. Tomic-Canic M, Perez-Perez GI, Blumenberg M (2014) Cutaneous microbiome studies in the times of affordable sequencing. J Dermatol Sci 75:82–87. doi: 10.1016/j.jdermsci.2014.05.001 PubMedCrossRefGoogle Scholar
  104. Troccaz M, Gaïa N, Beccucci S, Schrenzel J, Cayeux I, Starkenmann C, Lazarevic V (2015) Mapping axillary microbiota responsible for body odours using a culture-independent approach. Microbiome 3:3. doi: 10.1186/s40168-014-0064-3 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Urmacher C (1990) Histology of normal skin. Am J Surg Pathol 14:671–686PubMedCrossRefGoogle Scholar
  106. Verhulst NO, Qiu YT, Beijleveld H, Maliepaard C, Knights D, Schulz S, Berg-Lyons D, Lauber CL, Verduijn W, Haasnoot GW, Mumm R, Bouwmeester HJ, Claas FHJ, Dicke M, van Loon JJA, Takken W, Knight R, Smallegange RC (2011) Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLoS ONE 6:e28991. doi: 10.1371/journal.pone.0028991 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Wilke K, Martin A, Terstegen L, Biel SS (2007) A short history of sweat gland biology. Int J Cosmet Sci 29:169–179. doi: 10.1111/j.1467-2494.2007.00387.x PubMedCrossRefGoogle Scholar
  108. Williams RE, Gibson AG, Aitchison TC, Lever R, Mackie RM (1990) Assessment of a contact-plate sampling technique and subsequent quantitative bacterial studies in atopic dermatitis. Br J Dermatol 123:493–501PubMedCrossRefGoogle Scholar
  109. Wilson M (2008) Bacteriology of humans an ecological perspective. Blackwell Pub, MaldenGoogle Scholar
  110. Zeeuwen PLJM, Kleerebezem M, Timmerman HM, Schalkwijk J (2013) Microbiome and skin diseases. Curr Opin Allergy Clin Immunol 13:514–520. doi: 10.1097/ACI.0b013e328364ebeb PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Faculty of Medical and Life Sciences, Institute of Precision Medicine, Microbiology and Hygiene GroupFurtwangen UniversityVillingen-SchwenningenGermany
  2. 2.Corporate Scientific ServicesHenkel AG & Co. KGaADüsseldorfGermany

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