Skin microbiota: Microbial community structure and its potential association with health and disease

Infection, Genetics and Evolution

Volumn 11, Issue 5, 2011, Pages 839-848

  Rosenthal, Mariana ^a   Goldberg, Deborah ^b   Aiello, Allison ^a   Larson, Elaine ^c   Foxman, Betsy ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

Diversity; Epidemiology; Microbial ecology; Skin; Transmission

Indexed keywords

BACTERIAL TRANSMISSION; COMMUNITY STRUCTURE; DEMOGRAPHY; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; GENETIC ASSOCIATION; HAND WASHING; HEALTH BEHAVIOR; HOST PATHOGEN INTERACTION; HUMAN; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; NUCLEIC ACID HYBRIDIZATION; OUTCOME ASSESSMENT; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; PRIORITY JOURNAL; PUNCH BIOPSY; REVIEW; SAMPLING; SKIN CULTURE; SKIN FLORA; SKIN STRUCTURE;

BACTERIA; BIODIVERSITY; HUMANS; MICROBIAL INTERACTIONS; SKIN;

EID: 79956293726     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2011.03.022     Document Type: Review

References (88)

1. Aiello A.E., Cimiotti J., Della-Latta P., Larson E.L. A comparison of the bacteria found on the hands of 'homemakers' and neonatal intensive care unit nurses. J. Hosp. Infect. 2003, 54(4):310-315.
2. Aiello A.E., Coulborn R.M., Perez V., Larson E.L. Effect of hand hygiene on infectious disease risk in the community setting: a meta-analysis. Am. J. Public Health 2008, 98(8):1372-1381.
3. Allegranzi B., Pittet D. Role of hand hygiene in healthcare-associated infection prevention. Hosp. Infect. 2009, 73:305-315.
4. Bek-Thomsen M., Lomholt H.B., Kilian M. Acne is not associated with yet-uncultured bacteria. J. Clin. Microbiol. 2008, 46(10):3355-3360.
5. Benson A.K., Kelly S.A., Legge R., Ma F., Low S.J., Kim J., Zhang M., Oh P.L., Nehrenberg D., Hua K., Kachman S.D., Moriyama E.N., Walter J., Peterson D.A., Pomp D. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(44):18933-18938.
6. Borges L.F.A., Silva B.L., Filho P.P.G. Hand washing: changes in the skin flora. Am. J. Infect. Control 2007, 35:417-420.
7. Bowcock A.M., Woodson W.O.C.M. The genetics of psoriasis, psoriatic arthritis, and atopic dermatitis. Hum. Mol. Genet. 2004, 13(1):R43-R55.
8. Chang J.Y., Antonopoulos D.A., Kalra A., Tonelli A., Khalife W.T., Schmidt T.M., Young V.B. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J. Infect. Dis. 2008, 197:435-438.
9. Chiller K., Selkin B.A., Murakawa G.J. Skin microflora and bacterial infections of the skin. J. Invest. Dermatol. Symp. Proc. 2001, 6:170-174.
10. Cogen A.J., Nizet V., Gallo R.L. Skin microbiota: a source of disease or defence?. Brit. J. Dermatol. 2007, 158:442-455.
11. Correa M.C., Memije E.V., Vargas-Alarcón G., Guzmán R.A., Rosetti F., Acuña-Alonzo V., Martínez-Rodríguez N., Granados J. HLA-DR association with the genetic susceptibility to develop ashy dermatosis in Mexican Mestizo patients. J. Am. Acad. Dermatol. 2007, 56(4):617-620.
12. Costello E.K., Lauber C.L., Hamady M., Fierer N., Gordon J.I., Knight R. Bacterial community variation in human body habitats across space and time. Science 2009, 326:1694-1697.
13. Davies C.E., Wilson M.J., Hill K.E., Stephens P., Hill M., Harding K.G., Thomas D.W. Use of molecular techniques to study microbial diversity in the skin: chronic wounds reevaluated. Wound Rep. Reg. 2001, 9:332-340.
14. Dekio I., Hayashi H., Sakamoto M., Kitahara M., Nishikawa T., Suematsu M., Benno Y. Detection of potentially novel bacterial components of the human skin microbiota using culture-independent molecular profiling. J. Med. Microbiol. 2005, 54:1231-1238.
15. Dekio I., Sakamoto M., Hayashi H., Amagai M., Suematsu M., Benno Y. Characterization of skin microbiota in patients with atopic dermatitis and in normal subjects using 16S rRNA gene-based comprehensive analysis. J. Med. Microbiol. 2007, 56:1675-1683.
16. Delwart E.L. Viral metagenomics. Rev. Med. Virol. 2007, 17:115-131.
17. Dethlefsen L., Eckburg P.B., Bik E.M., Relman D.A. Assembly of the human intestinal microbiota. Trends Ecol. Evol. 2006, 21(9):517-523.
18. Diez Roux A.V., Aiello A.E. Multilevel analysis of infectious diseases. J. Infect. Dis. 2005, 191(Suppl. 1):S25-S33.
19. Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. 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(26):11971-11975.
20. Dotterud L.K., Wilsgaard T., Vorland L.H., Falk E.S. The effect of UVB radiation on skin microbiota in patients with atopic dermatitis and healthy controls. Int. J. Circumpolar Health 2008, 67(2-3):254-260.
21. Evans C.A. Persistent individual differences in the bacterial flora of the skin of the forehead: numbers of propionibacteria. J. Invest. Dermatol. 1975, 64:42-46.
22. Evans C.A., Crook J.R., Strom M.S. The bacterial flora of the forehead and back of Alaskan native villagers in summer and in winter. J. Invest. Dermatol. 1984, 82(3):294-297.
23. Feazel L.M., Baumgartner L.K., Peterson K.L., Frank D.N., Harris J.K., Pace N.R. Opportunistic pathogens enriched in showerhead biofilms. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(38):16393-16399.
24. Fernández L., Delgado S., Herrero H., Maldonado A., Rodríguez J.M. The bacteriocin nisin, an effective agent for the treatment of staphylococcal mastitis during lactation. J. Hum. Lact. 2008, 24(3):311-316.
25. 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. U.S.A. 2008, 105(46):17994-17999.
26. Foxman B., Goldberg D., Murdock C., Xi C., Gilsdorf J.R. Conceptualizing human microbiota: from multicelled organ to ecological community. Interdisciplinary Perspect. Infect. Dis. 2008, 1-5. Article ID 613979.
27. Fredricks D.N. Microbial ecology of human skin in health and disease. J. Invest. Dermatol. Symp. Proc. 2001, 6(3):167-169.
28. Gao Z., Tseng C., Pei Z., Blaser M.J. Molecular analysis of human forearm superficial skin bacterial biota. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(8):2927-2932.
29. Gao Z., Tseng C., Strober B.E., Pei Z., Blaser M.J. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One 2008, 3(7):e2719.
30. Grice E.A., Kong H.H., Renaud G., Young A.C., Bouffard G.G., Blakesley R.W., Wolfsberg T.G., Turner M.L., Segre J.A. A diversity profile of the human skin microbiota. Genome Res. 2008, 18:1043-1050.
31. Grice E.A., Kong H.H., Conlan S., Deming C.B., Davis J., Young A.C., Bouffard G.G., Blakesley R.W., Murray P.R., Green E.D., Turner M.L., Segre J.A. Topographical and temporal diversity of the human skin microbiome. Science 2009, 324:1190.
32. Hamady M., Knight R. Microbial community profiling for human microbiome projects: tools techniques, and challenges. Genome Res. 2009, 19(7):1141-1152.
33. Hrncir T., Stepankova R., Kozakova H., Hudcovic T., Tlaskalova-Hogenova H. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol. 2008, 9(65):1-11.
34. Iwase T., Uehara Y., Shinji H., Tajima A., Seo H., Takada K., Agata T., Mizunoe Y. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010, 465(7296):346-349.
35. Jha A.K., Gurung D. Seasonal variation of skin diseases in Nepal: a hospital-based annual study of out-patient visits. Nepal Med. Coll. J. 2006, 8(4):266-268.
36. Kaeberlein T., Lewis K., Epstein S.S. Isolating " uncultivable" microorganisms in pure culture in a simulated natural environment. Science 2002, 296(5570):1127-1129.
37. Kagan L.J., Aiello A.E., Larson E. The role of the home environment in the transmission of infectious diseases. J. Commun. Health 2002, 27(4):247-267.
38. Kampf G., Kramer A. Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin. Microbiol. Rev. 2004, 17(4):863-893.
39. Klaenhammer T.R. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 1993, 12(1-3):39-85.
40. Krutmann J. Pre- and probiotics for human skin. J. Dermatol. Sci. 2009, 54:1-5.
41. Lai Y., Di Nardo A., Nakatsuji T., Leichtle A., Yang Y., Cogen A.L., Wu Z.R., Hooper L.V., Schmidt R.R., von Aulock S., Radek K.A., Huang C.M., Ryan A.F., Gallo R.L. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 2009, 15(12):1377-1382.
42. Larson E.L., Cronquist A.B., Whittier S., Lai L., Lyle C.T., Della-Latta P. Differences in skin flora between inpatients and chronically ill outpatients. Heart Lung 2000, 29(4):298-305.
43. Larson E. Hygiene of the skin: when is clean too clean?. Emerg. Infect. Dis. 2001, 7(2):225-230.
44. Larson E.L., Gomez-Duarte C., Lee L.V., Della-Latta P., Kain D.J., Keswick B.H. Microbial flora of hands of homemakers. Am. J. Infect. Control. 2002, 31(2):72-79.
45. Larson E.L., Lin S.X., Gomez-Pichardo C., Della-Latta P. Effect of antibacterial home cleaning and handwashing products on infectious disease symptoms: a randomized, double-blind trial. Ann. Intern. Med. 2004, 140(5):321-329.
46. Little A.E.F., Robinson C.J., Peterson S.B., Raffa K.F., Handelsman J. Rules of engagement: interspecies interactions that regulate microbial communities. Ann. Rev. Microbiol. 2008, 62:375-401.
47. Lo C.W., Lai Y.K., Liu Y.T., Gallo R.L., Huang C.M. Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting β-hemolysin and CAMP factor. J. Invest. Dermatol. 2010, [Epub ahead of print].
48. Luby S.P., Agboatwalla M., Feikin D.R., Painter J., Billhimer W.M.S., Altaf A., Hoekstra R.M. Effect of handwashing on child health: a randomised controlled trial. Lancet 2005, 366:225-233.
49. Mai V., Draganov P.V. Recent advances and remaining gaps in our knowledge of associations between gut microbiota and human health. World J. Gastroenterol. 2009, 15(1):81-85.
50. Maier R.M., Palmer M.W., Andersen G.L., Halonen M.J., Josephson K.C., Maier R.S., Martinez F.D., Neilson J.W., Stern D.A., Vercelli D., Wright A.L. The bacterial community in household dust: environmental determinants and impact on childhood asthma. Appl. Environ. Microbiol. 2010, 76(8):2663-2667.
51. Marris E. Staving Off Ecological Disaster in Lungs 2009, http://www.nature.com/news/2009/090807/full/news.2009.808.html.
52. Martin-Visscher L.A, van Belkum M.J., Garneau-Tsodikova S., Whittal R.M., Zheng J., McMullen L.M., Vederas J.C. Isolation and characterization of carnocyclin a, a novel circular bacteriocin produced by Carnobacterium maltaromaticum UAL307. Appl Environ Microbiol. 2008, 74(15):4756-4763.
53. Marshall B.M., Ochieng D.J., Levy S.B. Commensals: underappreciated reservoir of antibiotic resistance. Microbe 2008, 4(5):231-238.
54. Masenga J., Garbe C., Wagner J., Orfanos C.E. Staphylococcus aureus in atopic dermatitis and in nonatopic dermatitis. Int. J. Dermatol. 1990, 29(8):579-582.
55. McBride M.E., Duncan W.C., Knowx J.M. Cutaneous microflora of patients with repeated skin infections. J. Cutaneous Pathol. 1977, 4:14-22.
56. McGuire A.L., Colgrove J., Whitney S.N., Diaz C.M., Bustillos D., Versalovic J. Ethical, legal, and social considerations in conducting the Human Microbiome Project. Genome Res. 2008, 18:1861-1864.
57. Nakabayashi A., Sei Y., Guillot J. Identification of Malassezia species isolated from patients with seborrhoeic dermatitis, atopic dermatitis, pityriasis versicolor and normal subjects. Med. Mycol. 2000, 38:337-341.
58. Oakley B.B., Fiedler T.L., Marrazzo J.M., Fredricks D.N. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl. Environ. Microbiol. 2008, 74(15):4898-4909.
59. Ogunseitan O. Microbial Diversity 2005, Blackwell Publishing, Malden, MA.
60. Oh S., Kim S.H., Ko Y., Sim J.H., Kim K.S., Lee S.H., Park S., Kim Y.J. Effect of bacteriocin produced by Lactococcus sp, HY 449 on skin-inflammatory bacteria. Food Chem. Toxicol. 2006, 44:1184-1190.
61. Ordovas J.M., Mooser V. Metagenomics: the role of the microbiome in cardiovascular diseases. Curr. Opin. Lipidol. 2006, 17:157-161.
62. Othman M., Aguero R., Lin H.C. Alterations in intestinal microbial flora and human disease. Curr. Opin. Gastroenterol. 2008, 24:11-16.
63. Ott S.J., Kühbacher T., Musfeldt M., Rosenstiel P., Hellmig S., Rehman A., Drews O., Weichert W., Timmis K.N., Schreiber S. Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand. J. Gastroenterol. 2009, 43:831-841.
64. Otto M., Echner H., Voelter W., Götz F. Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 2001, 69(3):1957-1960.
65. Ouwehand A.C., Batsman A., Salminen S. Probiotics for the skin: a new area of potential application?. Lett. Appl. Microbiol. 2003, 36:327-331.
66. 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. 2006, 44(8):2933-2941.
67. Peterson J., Garges S., Giovanni M., et al. The NIH Human Microbiome Project. Genome Res. 2009, 19(12):2317-2323.
68. Pivarcsi A., Nagy I., Kemeny L. Innate immunity in the skin: how keratinocytes fight against pathogens. Curr. Immunol. Rev. 2005, 1:29-42.
69. Price L.B., Liu C.M., Johnson K.E., Aziz M., Lau M.K., Bowers J., Ravel J., Keim P.S., Serwadda D., Wawer M.J., Gray R.H. The effects of circumcision on the penis microbiome. PLoS One 2010, 5(1):1-12.
70. Rintala H., Pitkäranta M., Toivola M., Paulin L., Nevalainen A. Diversity and seasonal dynamics of bacterial community in indoor environment. BMC Microbiol. 2008, 8(56):1-13.
71. Romero-Steiner S., Witek T., Balish E. Adherence of skin bacteria to human epithelial cells. J. Clin. Microbiol. 1990, 28(1):27-31.
72. Roth R.R., James W.D. Microbial ecology of the skin. Ann. Rev. Microbiol. 1988, 42:441-461.
73. Sawa N., Zendo T., Kiyofuji J., Fujita K., Himeno K., Nakayama J., Sonomoto K. Identification and characterization of lactocyclicin Q, a novel cyclic bacteriocin produced by Lactococcus sp. strain QU 12. Appl. Environ. Microbiol. 2009, 75(6):1552-1558.
74. Scharschmidt T.C., List K., Grice E.A., Szabo R., NISC Comparative Sequencing Program, Renaud G., Lee C.C., Wolfsberg T.G., Bugge T.H., Segre J.A. Matriptase-deficient mice exhibit ichthyotic skin with a selective shift in skin microbiota. J. Invest. Dermatol. 2009, 129(10):2435-2442.
75. Selwyn S. Natural antibiosis among skin bacteria as a primary defence against infection. Brit. J. Dermatol. 1975, 93:487-493.
76. Singh S., Kaye S., Gore M.E., McClure M.O., Bunker C.B. The role of human endogenous retroviruses in melanoma. Brit. J. Dermatol. 2009, 161:1225-1231.
77. Sommer M.O.A., Dantas G., Church G.M. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 2009, 325:1128-1131.
78. Stecher B., Hardt W.D. The role of microbiota in infectious disease. Trends Microbiol. 2008, 16(3):107-114.
79. Sultana B., Cimiotti J., Aiello A.E., Sloan D., Larson E. Effects of age and race on skin condition and bacterial counts on hands of neonatal ICU nurses. Heart Lung. 2003, 32(4):283-289.
80. Theron J., Cloete T.E. Molecular techniques for determining microbial diversity and community structure in natural environments. Crit. Rev. Microbiol. 2000, 26(1):37-57.
81. Tiwari S.K., Srivastava S. Purification and characterization of plantaricin LR14: a novel bacteriocin produced by Lactobacillus plantarum LR/14. Appl. Microbiol. Biotechnol. 2008, 79(5):759-767.
82. Tlaskalová-Hogenová H., Štepánková R., Hudcovic T., Tucková L., Cukrowska B., Lodinová-Žádni{dotless}ková R., Kozáková H., Rossmanna P., Bártová J., Sokol D., Funda D.P., Borovská D., Reháková Z., Šinkora J., Hofman J., Drastich P., Kokešová A. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol. Lett. 2004, 93:97-108.
83. van Belkum A., Melles D.C., Nouwen J., van Leeuwen W.B., van Wamel W., Vos M.C., Wertheim H.F.L., Verbrugh H.A. Co-evolutionary aspects of human colonization and infection by Staphylococcus aureus. Infect. Genet. Evol. 2009, 9:32-47.
84. Wanke I., Steffen H., Christ C., Krismer B., Götz F., Peschel A., Schaller M., Schittek B. Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J. Invest. Dermatol. 2010, [Epub ahead of print].
85. Wilson M. Microbial Inhabitants of Humans: Their Ecology and Role in Health and Disease 2005, Cambridge University Press, Cambridge. first ed.
86. Wilson M. Bacteriology of Humans: An Ecological Perspective 2008, Blackwell Publishing, Oxford. first ed.
87. Wright P., Terry C.S. Antagonism within populations of micro-organisms from normal human skin. J. Med. Microbiol. 1981, 14:271-278.
88. Young V.B., Britton R.A., Schmidt T.M. The human microbiome and infectious diseases: beyond Koch. Interdisciplinary Perspect. Infect. Dis. 2008, 2008:1-2. Article ID 296873.