Advertisement
Journal of Investigative Dermatology Home

Shifts in the Skin Bacterial and Fungal Communities of Healthy Children Transitioning through Puberty

  • Jin Park
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA

    Department of Dermatology, Jeonbuk National University Medical School, Jeonju, Korea

    Research Institute of Clinical Medicine of Jeonbuk National University – Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, Korea
    Search for articles by this author
  • Nicole H. Schwardt
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Jay-Hyun Jo
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Zhiwei Zhang
    Affiliations
    Biostatistics Branch, Division of Cancer Treatment and Diagnostics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Valentina Pillai
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Sheila Phang
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Sheila M. Brady
    Affiliations
    Section on Growth and Obesity, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Jessica A. Portillo
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Margaret A. MacGibeny
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA

    Rutgers Robert Wood Johnson Medical School, Piscataway, New Jersey, USA
    Search for articles by this author
  • Hai Liang
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Meridith Pensler
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Steven J. Soldin
    Affiliations
    Department of Laboratory Medicine, Clinical Center, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Jack A. Yanovski
    Affiliations
    Section on Growth and Obesity, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Julia A. Segre
    Affiliations
    Translational and Functional Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
  • Heidi H. Kong
    Correspondence
    Correspondence: Heidi H. Kong, Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
    Affiliations
    Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA
    Search for articles by this author
      Previous cross-sectional studies have shown that skin microbiomes in adults are distinct from those in children. However, the human skin microbiome in individuals as they sexually mature has not been studied as extensively. We performed a prospective, longitudinal study to investigate the puberty-associated shifts in skin microbiota. A total of 12 healthy children were evaluated every 6–18 months for up to 6 years. Using 16S ribosomal RNA (V1–V3) and internal transcribed spacer 1 amplicon sequencing analyzed with Divisive Amplicon Denoising Algorithm 2, we characterized the bacterial and fungal communities of five different skin and nares sites. We identified significant alterations in the composition of skin microbial communities, transitioning toward a more adult microbiome, during puberty. The microbial shifts were associated with Tanner stages (classification method for the degree of sexual maturation) and showed noticeable sex-specific differences. Over time, female children demonstrated a predominance of Cutibacterium with decreasing diversity. Among fungi, Malassezia predominated at most skin sites in more sexually mature subjects, which was more pronounced in female children. The higher relative abundances of these lipophilic taxa—C. acnes and M. restricta—were strongly associated with serum sex hormone concentrations with known influence on sebaceous gland activity. Taken together, our results support the relationship between sexual maturation, skin physiology, and the skin microbiome.

      Abbreviations:

      Ac (antecubital fossa), DAD2 (Divisive Amplicon Denoising Algorithm 2), Fh (forehead), ITS (internal transcribed spacer), Ra (retroauricular crease), Vf (volar forearm)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      PDF Download and 24 Hours Online Access
      Society Members (SID/ESDR), remember to log in for access.

      Subscribe:

      Subscribe to Journal of Investigative Dermatology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Callahan B.J.
        • McMurdie P.J.
        • Rosen M.J.
        • Han A.W.
        • Johnson A.J.
        • Holmes S.P.
        DADA2: high-resolution sample inference from Illumina amplicon data.
        Nat Methods. 2016; 13: 581-583
        • Capone K.A.
        • Dowd S.E.
        • Stamatas G.N.
        • Nikolovski J.
        Diversity of the human skin microbiome early in life.
        J Invest Dermatol. 2011; 131: 2026-2032
        • Cole J.R.
        • Wang Q.
        • Fish J.A.
        • Chai B.
        • McGarrell D.M.
        • Sun Y.
        • et al.
        Ribosomal Database Project: data and tools for high throughput rRNA analysis.
        Nucleic Acids Res. 2014; 42: D633-D642
        • 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
        • Excoffier L.
        • Smouse P.E.
        • Quattro J.M.
        Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.
        Genetics. 1992; 131: 479-491
        • Fadrosh D.W.
        • Ma B.
        • Gajer P.
        • Sengamalay N.
        • Ott S.
        • Brotman R.M.
        • et al.
        An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform.
        Microbiome. 2014; 2: 6
        • 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. 2008; 105: 17994-17999
        • Findley K.
        • Oh J.
        • Yang J.
        • Conlan S.
        • Deming C.
        • Meyer J.A.
        • et al.
        Topographic diversity of fungal and bacterial communities in human skin.
        Nature. 2013; 498: 367-370
        • Giacomoni P.U.
        • Mammone T.
        • Teri M.
        Gender-linked differences in human skin.
        J Dermatol Sci. 2009; 55: 144-149
        • Grice E.A.
        • Kong H.H.
        • Conlan S.
        • Deming C.B.
        • Davis J.
        • Young A.C.
        • et al.
        Topographical and temporal diversity of the human skin microbiome.
        Science. 2009; 324: 1190-1192
        • Hickey R.J.
        • Zhou X.
        • Settles M.L.
        • Erb J.
        • Malone K.
        • Hansmann M.A.
        • et al.
        Vaginal microbiota of adolescent girls prior to the onset of menarche resemble those of reproductive-age women.
        mBio. 2015; 6: e00097-e00115
        • Jo J.H.
        • Deming C.
        • Kennedy E.A.
        • Conlan S.
        • Polley E.C.
        • Ng W.I.
        • et al.
        Diverse human skin fungal communities in children converge in adulthood.
        J Invest Dermatol. 2016; 136: 2356-2363
        • 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. 1975; 65: 379-381
        • Liang K.Y.
        • Zeger S.L.
        Longitudinal data analysis using generalized linear models.
        Biometrika. 1986; 73: 13-22
        • Lynn D.D.
        • Umari T.
        • Dunnick C.A.
        • Dellavalle R.P.
        The epidemiology of acne vulgaris in late adolescence.
        Adolesc Health Med Ther. 2016; 7: 13-25
        • Marples R.R.
        Sex, constancy, and skin bacteria.
        Arch Dermatol Res. 1982; 272: 317-320
        • Marshall W.A.
        • Tanner J.M.
        Variations in pattern of pubertal changes in girls.
        Arch Dis Child. 1969; 44: 291-303
        • Marshall W.A.
        • Tanner J.M.
        Variations in the pattern of pubertal changes in boys.
        Arch Dis Child. 1970; 45: 13-23
        • McGinley K.J.
        • Webster G.F.
        • Ruggieri M.R.
        • Leyden J.J.
        Regional variations in density of cutaneous propionibacteria: correlation of Propionibacterium acnes populations with sebaceous secretion.
        J Clin Microbiol. 1980; 12: 672-675
        • Nilsson R.H.
        • Larsson K.H.
        • Taylor A.F.S.
        • Bengtsson-Palme J.
        • Jeppesen T.S.
        • Schigel D.
        • et al.
        The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications.
        Nucleic Acids Res. 2019; 47: D259-D264
        • Oh J.
        • Conlan S.
        • Polley E.C.
        • Segre J.A.
        • Kong H.H.
        Shifts in human skin and nares microbiota of healthy children and adults.
        Genome Med. 2012; 4: 77
        • O’Leary N.A.
        • Wright M.W.
        • Brister J.R.
        • Ciufo S.
        • Haddad D.
        • McVeigh R.
        • et al.
        Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation.
        Nucleic Acids Res. 2016; 44: D733-D745
        • O'Neill A.M.
        • Gallo R.L.
        Host-microbiome interactions and recent progress into understanding the biology of acne vulgaris.
        Microbiome. 2018; 6: 177
        • Paller A.S.
        • Kong H.H.
        • Seed P.
        • Naik S.
        • Scharschmidt T.C.
        • Gallo R.L.
        • et al.
        The microbiome in patients with atopic dermatitis [published correction appears in J Allergy Clin Immunol 2019;143:1660].
        J Allergy Clin Immunol. 2019; 143: 26-35
        • Pochi P.E.
        • Strauss J.S.
        • Downing D.T.
        Age-related changes in sebaceous gland activity.
        J Invest Dermatol. 1979; 73: 108-111
        • Ramasastry P.
        • Downing D.T.
        • Pochi P.E.
        • Strauss J.S.
        Chemical composition of human skin surface lipids from birth to puberty.
        J Invest Dermatol. 1970; 54: 139-144
        • Ro B.I.
        • Dawson T.L.
        The role of sebaceous gland activity and scalp microfloral metabolism in the etiology of seborrheic dermatitis and dandruff.
        J Investig Dermatol Symp Proc. 2005; 10: 194-197
        • Shi B.
        • Bangayan N.J.
        • Curd E.
        • Taylor P.A.
        • Gallo R.L.
        • Leung D.Y.M.
        • et al.
        The skin microbiome is different in pediatric versus adult atopic dermatitis.
        J Allergy Clin Immunol. 2016; 138: 1233-1236
        • Somerville D.A.
        The normal flora of the skin in different age groups.
        Br J Dermatol. 1969; 81: 248-258
        • Staudinger T.
        • Pipal A.
        • Redl B.
        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. 2011; 110: 1381-1389
        • Strauss J.S.
        • Kligman A.M.
        • Pochi P.E.
        The effect of androgens and estrogens on human sebaceous glands.
        J Invest Dermatol. 1962; 39: 139-155
        • Sugita T.
        • Suzuki M.
        • Goto S.
        • Nishikawa A.
        • Hiruma M.
        • Yamazaki T.
        • et al.
        Quantitative analysis of the cutaneous Malassezia microbiota in 770 healthy Japanese by age and gender using a real-time PCR assay.
        Med Mycol. 2010; 48: 229-233
        • Yuan X.
        • Chen R.
        • Zhang Y.
        • Lin X.
        • Yang X.
        Gut microbiota: effect of pubertal status.
        BMC Microbiol. 2020; 20: 334
        • Zouboulis C.C.
        • Chen W.C.
        • Thornton M.J.
        • Qin K.
        • Rosenfield R.
        Sexual hormones in human skin.
        Horm Metab Res. 2007; 39: 85-95