Research ArticleMICROBIAL ECOLOGY

Staphylococcus aureus and the ecology of the nasal microbiome

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Science Advances  05 Jun 2015:
Vol. 1, no. 5, e1400216
DOI: 10.1126/sciadv.1400216
  • Fig. 1 The seven nasal CSTs and their respective bacterial densities shown in boxplots and composition shown in heatmap visualization and non-metric multidimensional scaling (nMDS) ordination plot.

    (A) In the boxplots, the box of each boxplot denotes the IQR (Q2-Q3) and the corresponding median, whereas the whiskers signify the upper and lower 1.5 × IQR, and the open circles denote outliers beyond the whiskers. The difference in bacterial density was significantly greater across than within CSTs [analysis of variance (ANOVA), P < 0.001]. In particular, CST3 had significantly lower bacterial density than all other CSTs except CST4, and CST2 had significantly higher bacterial density than all other CSTs except CST6 (two-tailed Wilcoxon rank sum, P < 0.05) (A). (B) In the heatmap visualization, each participant’s nasal microbiota is represented in a single column, and proportional abundance of each nasal bacterial taxon is shown by row according to the color key to the left. The nasal microbiota is grouped by CSTs, as indicated by the CST color bar above. The S. aureus culture result of each participant is noted by the green/black color bar above. (C) In the nMDS ordination plot, each participant’s nasal microbiota (in proportional abundance) is represented by a single data point, and data points that are closer have a more similar composition than those that are farther apart. The centroids and 95% confidence ellipse for each CST are shown.

  • Fig. 2 Nasal bacterial density and S. aureus absolute abundance by sex and the relationship between S. aureus absolute abundance and S. aureus culture.

    (A) The scatterplot shows the higher nasal bacterial density in men than in women. Individuals (non-CST1) with detectable S. aureus nasal colonization could be divided on the basis of S. aureus absolute abundance into four categories. (B) Women were more likely to have the two lowest categories of S. aureus absolute abundance (that is, <104 and 104-105), whereas men are more likely to have the middle two categories (that is, 104-105 and 105-106). (C) Culture outcome was strongly linked to S. aureus absolute abundance, and each 10-fold increase in S. aureus absolute abundance increases the probability of positive S. aureus culture by 30%, which suggests that the sex difference in S. aureus absolute abundance might explain the lower S. aureus culture rates in women than in men.

  • Fig. 3 Results from decision tree model derivation and validation showing threshold-dependent relationships between the absolute abundances of nasal commensals and S. aureus presence/absence.

    (A) Model predicting S. aureus presence/absence was derived using a randomly drawn group of 100; it showed that the most informative split was a threshold of 1.2 × 106 Dolosigranulum 16S rRNA gene copies per swab. Having above-threshold Dolosigranulum predicts absence of S. aureus (n = 4/25, 16.0%), as compared to S. aureus nasal colonization rate in the overall derivation group (n = 56/100, 56%). Simonsiella had a similarly negative relationship to S. aureus, where, among individuals who had below-threshold abundance of Dolosigranulum, having ≥1.1 × 105 Simonsiella predicts the absence of S. aureus (n = 1/7, 14.3%). (B) Validation testing using 10 randomly drawn groups of 100 supported the threshold-based relationships between Dolosigranulum, Simonsiella, P. granulosum, and S. epidermidis and S. aureus presence/absence.

  • Table 1 Participant demographics and characteristics.

    Monozygotic
    (n = 46 pairs)
    Dizygotic
    Same sex
    (n = 23 pairs)
    Opposite sex
    (n = 20 pairs)
    Number of individuals or twin pairs (%)
    Age (years)
      50–5412 (26.1)0 (0.0)0 (0.0)
      55–5913 (28.3)0 (0.0)0 (0.0)
      60–647 (15.2)4 (17.4)1 (5.0)
      65–699 (19.6)4 (17.4)11 (55.0)
      70–743 (6.5)12 (52.2)7 (35.0)
      75–792 (4.4)3 (13.0)1 (5.0)
    Sex
      Female25 (54.4)16 (69.6)20 (100.0)
      Male21 (45.6)7 (30.4)
    Smoking
      Smoker14 (15.2)9 (19.6)10 (25.0)
      Concordance40 (87.0)16 (69.6)12 (60.0)
    History of atopic disease*
      Yes27 (29.3)14 (30.4)13 (32.5)
      Concordance29 (63.0)15 (65.2)11 (55.0)
    History of psoriasis
      Yes8 (8.7)2 (4.3)5 (12.5)
      Unknown2 (2.2)1 (2.2)2 (5.0)
      Concordance38 (82.6)20 (87.0)13 (65.0)
    Farm exposure
      Yes1 (1.1)2 (4.3)1 (2.5)
      Unknown0 (0.0)2 (4.3)0 (0.0)
      Concordance45 (97.8)21 (91.3)19 (95.0)

    *Atopic diseases include asthma, atopic dermatitis, and allergy.

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/5/e1400216/DC1

      Fig. S1. Correlation of nasal microbiota composition among monozygotic and among same-sex and opposite-sex dizygotic twin pairs in non-metric multidimensional scaling ordination plots.

      Fig. S2. Rates of S. aureus nasal colonization by sequencing and by culture and S. aureus absolute abundance for the seven nasal CSTs.

      Fig. S3. Results from decision tree model derivation and validation showing threshold-dependent relationships between the absolute abundances of nasal commensals and S. aureus.

      Table S1. The indicator genera for each nasal CST identified on the basis of proportional abundance, where CI < 0.80 denotes bacteria taxa assigned with <80% bootstrap confidence level.

      Table S2. Nasal bacterial density (median and IQR) of each nasal CST and the prevalence of each CST by sex.

      Table S3. Comparison of within-twin nasal microbiota composition correlation between monozygotic and dizygotic twins based on pairwise ecological distance (Jaccard, Bray-Curtis, and Euclidean distances).

      Table S4. Results from standard biometrical heritability analysis using a polygenic model to determine the contribution of additive genetic effects (A), genetics effects due to dominance (D), shared environmental effects (C), and nonshared environmental effects (E) to nasal bacterial density.

      Table S5. The associations between nasal bacterial density and host factors, including sex, assessed by Wilcoxon rank sum and Kolmogorov-Smirnov tests.

      Table S6. Comparison of nasal bacterial density by sex, adjusted for nasal CST in a quasi-Poisson model.

      References (2533)

    • Supplementary Materials

      This PDF file includes:

      • Fig. S1. Correlation of nasal microbiota composition among monozygotic and among same-sex and opposite-sex dizygotic twin pairs in non-metric multidimensional scaling ordination plots.
      • Fig. S2. Rates of S. aureus nasal colonization by sequencing and by culture and S. aureus absolute abundance for the seven nasal CSTs.
      • Fig. S3. Results from decision tree model derivation and validation showing threshold-dependent relationships between the absolute abundances of nasal commensals and S. aureus.
      • Table S1. The indicator genera for each nasal CST identified on the basis of proportional abundance, where CI < 0.80 denotes bacteria taxa assigned with <80% bootstrap confidence level.
      • Table S2. Nasal bacterial density (median and IQR) of each nasal CST and the prevalence of each CST by sex.
      • Table S3. Comparison of within-twin nasal microbiota composition correlation between monozygotic and dizygotic twins based on pairwise ecological distance (Jaccard, Bray-Curtis, and Euclidean distances).
      • Table S4. Results from standard biometrical heritability analysis using a polygenic model to determine the contribution of additive genetic effects (A), genetics effects due to dominance (D), shared environmental effects (C), and nonshared environmental effects (E) to nasal bacterial density.
      • Table S5. The associations between nasal bacterial density and host factors, including sex, assessed by Wilcoxon rank sum and Kolmogorov-Smirnov tests
        Table S6. Comparison of nasal bacterial density by sex, adjusted for nasal CST in a quasi-Poisson model.
      • References (2533)

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