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. 2015 Jun 5;1(5):e1400216.
doi: 10.1126/sciadv.1400216. eCollection 2015 Jun.

Staphylococcus aureus and the ecology of the nasal microbiome

Cindy M Liu  1 , Lance B Price  2 , Bruce A Hungate  3 , Alison G Abraham  4 , Lisbeth A Larsen  5 , Kaare Christensen  6 , Marc Stegger  7 , Robert Skov  8 , Paal Skytt Andersen  9
Affiliations

Staphylococcus aureus and the ecology of the nasal microbiome

Cindy M Liu et al. Sci Adv. .

Abstract

The human microbiome can play a key role in host susceptibility to pathogens, including in the nasal cavity, a site favored by Staphylococcus aureus. However, what determines our resident nasal microbiota-the host or the environment-and can interactions among nasal bacteria determine S. aureus colonization? Our study of 46 monozygotic and 43 dizygotic twin pairs revealed that nasal microbiota is an environmentally derived trait, but the host's sex and genetics significantly influence nasal bacterial density. Although specific taxa, including lactic acid bacteria, can determine S. aureus colonization, their negative interactions depend on thresholds of absolute abundance. These findings demonstrate that nasal microbiota is not fixed by host genetics and opens the possibility that nasal microbiota may be manipulated to prevent or eliminate S. aureus colonization.

Keywords: Staphylococcus aureus; absolute abundance; competition; human microbiome; interspecies interaction; microbial ecology; microbiome; nares; nasal cavity; nasal microbiome.

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Figures

Fig. 1
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
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
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.
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