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Shifts in Human Skin and Nares Microbiota of Healthy Children and Adults Julia Oh1, Sean Conlan1, Eric C Polley2, Julia a Segre1*† and Heidi H Kong3*†

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Shifts in Human Skin and Nares Microbiota of Healthy Children and Adults Julia Oh1, Sean Conlan1, Eric C Polley2, Julia a Segre1*† and Heidi H Kong3*† Oh et al. Genome Medicine 2012, 4:77 http://genomemedicine.com/content/4/10/77 RESEARCH Open Access Shifts in human skin and nares microbiota of healthy children and adults Julia Oh1, Sean Conlan1, Eric C Polley2, Julia A Segre1*† and Heidi H Kong3*† Abstract Background: Characterization of the topographical and temporal diversity of the microbial collective (microbiome) hosted by healthy human skin established a reference for studying disease-causing microbiomes. Physiologic changes occur in the skin as humans mature from infancy to adulthood. Thus, characterizations of adult microbiomes might have limitations when considering pediatric disorders such as atopic dermatitis (AD) or issues such as sites of microbial carriage. The objective of this study was to determine if microbial communities at several body sites in children differed significantly from adults. Methods: Using 16S-rRNA gene sequencing technology, we characterized and compared the bacterial communities of four body sites in relation to Tanner stage of human development. Body sites sampled included skin sites characteristically involved in AD (antecubital/popliteal fossae), a control skin site (volar forearm), and the nares. Twenty-eight healthy individuals aged from 2 to 40 years were evaluated at the outpatient dermatology clinic in the National Institutes of Health’s Clinical Center. Exclusion criteria included the use of systemic antibiotics within 6 months, current/prior chronic skin disorders, asthma, allergic rhinitis, or other chronic medical conditions. Results: Bacterial communities in the nares of children (Tanner developmental stage 1) differed strikingly from adults (Tanner developmental stage 5). Firmicutes (Streptococcaceae), Bacteroidetes, and Proteobacteria (b, g) were overrepresented in Tanner 1 compared to Tanner 5 individuals, where Corynebacteriaceae and Propionibacteriaceae predominated. While bacterial communities were significantly different between the two groups in all sites, the most marked microbial shifts were observed in the nares, a site that can harbor pathogenic species, including Staphylococcus aureus and Streptococcus pneumonia. Conclusions: Significant shifts in the microbiota associated with progressive sexual maturation as measured by Tanner staging suggest that puberty-dependent shifts in the skin and nares microbiomes may have significant implications regarding prevention and treatment of pediatric disorders involving microbial pathogens and colonization. Background healthy human skin microbiome demonstrated vast com- Studies of microbial diseases typically focus on individual plexity and diversity [2,3] influenced by both environ- pathogens as causative agents. Recent insights into the mental and host factors. The influence of sexual microbial communities inhabiting the human body sug- maturation on the human skin microbiome is not well gest that pathogenicity can be enhanced or impaired by studied, but may have a profound effect on disease predi- shifts in bacterial communities and that disturbance in lection and outcome. the microbial ecosystem (dysbiosis) can contribute to dis- Maturation-dependent shifts in the skin microbiome ease [1]. Genomic sequencing surveys of the normal may be relevant to the prevention, diagnosis, and treat- ment strategies for disorders such as atopic dermatitis * Correspondence: [email protected]; [email protected] (AD) that differ in incidence and severity as individuals † Contributed equally 1Genetics and Molecular Biology Branch, National Human Genome Research physiologically mature. Prior studies have characterized Institute, NIH, 49 Convent Dr., Bethesda, MD 20814, USA 3Dermatology Branch, Center for Cancer Research, National Cancer Institute, NIH, 10 Center Dr., Bethesda, MD 20814, USA Full list of author information is available at the end of the article © 2012 Oh et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Oh et al. Genome Medicine 2012, 4:77 Page 2 of 11 http://genomemedicine.com/content/4/10/77 primarily cultivatable microbes [4,5] on the skin of sub- Culture collection jects of different ages, but cultivation techniques have Nasal Staphylococcus aureus cultures were performed by limited capacity to characterize fastidious or uncultivable the Department of Laboratory Medicine (DLM), Clinical organisms, which may represent upwards of 99% of bac- Center, NIH. Cultures were obtained with swabs (BBLtm teria [6]. In contrast, genomic studies, including metage- CultureSwab™, made by Copan for Becton, Dickinson nomic or 16S-ribosomal RNA sequence analysis, greatly and Company, Sparks, MD, USA) and plated on three dif- increase the range of detectable microbes. The 16S-rRNA ferent growth media: chocolate agar, trypticase soy agar gene is present in all bacteria/archaea and contains both with 5% sheep blood, and mannitol salt agar (Remel Pro- variable regions, which enable taxonomic classification, ducts, Lenexa, KS, USA). After overnight incubation at and conserved regions, which serve as universal binding 37°C, colonies were counted and assessed macroscopically sites for PCR primers. Such methods have been used to and also microscopically following staining by Gram’s investigate the healthy adult [2,3] and the neonatal skin stain. Identification was confirmed using Staphaurex microbiomes [7,8], but differences in the composition and agglutination reagent (Remel Products) or standard coagu- complexity of the skin microbiome as a result of major lase test. Culture results were returned as an assignment developmental stages such as puberty have not been to one of four categorical levels based on number of colo- explored. nies per sample: 0 (zero), 1 (scant), 2 (light), 3 (moderate), Progression from infancy to adulthood encompasses or 4 (heavy), corresponding to 0, 1, 2 to 10, 11 to 40, major biological changes with significant physiologic and or >40 colonies on a culture plate. endocrinologic skin alterations that, in turn, likely influ- ence the host-microbiome relationship. Since chronologi- Sample collection and processing cal age does not necessarily correspond with a defined All samples were collected (HHK) as described [2,12]. stage in sexual maturation [9,10], use of Tanner staging of Briefly, skin preparation instructions included avoidance sexual maturity can provide a phenotypic assessment of of bathing for 24 hours, emollients, antimicrobial soaps, or the physiologic age of an individual. This study describes shampoos for 7 days prior to all sampling. Sampling sites dramatic differences in the nares and skin microbiomes included the nares (N), antecubital fossa (Af), volar fore- that occur in younger children (Tanner stage 1) versus arm (Vf), and popliteal fossa (Pf). From a 4 cm2 area, bac- adults (Tanner stage 5), with a smaller number of children terial swabs (via Epicentre swabs) and scrapes (via sterile in intermediate Tanner groups (stages 2 to 4) suggestive of disposable surgical blade) were obtained and incubated in a microbial shift occuring around puberty. Researchers enzymatic lysis buffer and lysozyme for 30 minutes at 37° should consider these physiologic differentials when C. For the nares, only swab samples were taken. Scrapes designing and conducting investigations and developing and swabs were obtained from the other sites as available. interventions that promote healthy microbiomes. Correlation analysis of log proportions of genera identified in scrape versus swab sampling confirmed the similarity of Materials and methods techniques (R = 0.87, P<2.2 × 10-16, data not shown). Subjects Preparation of samples for Sanger sequencing Subjects were 28 healthy individuals (no systemic antibio- For the Tanner stages 1 to 4 samples, genomic DNA was tics within 6 months, no current or prior chronic skin dis- extracted with slight modifications to the original protocol orders, chronic medical conditions, asthma, or allergic used for the Tanner 5 subject samples [2,12], including a rhinitis, ascertained via an International Study of Asthma change in the enzymatic lysis buffer (Epicentre and Allergies in Childhood questionnaire [11]) ranging in MPY80200) and lysozyme (Epicentre R1802M), increase age from 2 to 40 years (Table S1 in Additional file 1). Data in the frequency and the duration of bead-beating (30 Hz, were analyzed retrospectively from our previous skin survey 2 minutes), higher heating temperature of the sample of healthy adults [2] with the addition of two samples. (65°C), purification with Invitrogen columns, and reduced Children (aged 2 to 17 years) were recruited into a prospec- dilution of the eluate (to 35 μl). Full-length 16S-rRNA tive longitudinal study approved by the institutional review genes from genomic extractions were PCR amplified using board of NHGRI, NIH for the study of children with AD the primer set 8F and 1391R, purified, cloned, and and healthy age-matched controls [12] with written sequenced at the National Institutes of Health Intramural informed consent obtained from the parents or guardians Sequencing Center (NISC) as described; 300 to 400 unique of all participating minors. All subjects were recruited from sequences were obtained from 16S amplicons of each clin- the local Washington, DC metropolitan region. The Tanner ical sample. To ensure that bias was not introduced
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