Clin Exp Otorhinolaryngol.  2022 Nov;15(4):335-345. 10.21053/ceo.2021.01928.

Compositional Alterations of the Nasal Microbiome and Staphylococcus aureus–Characterized Dysbiosis in the Nasal Mucosa of Patients With Allergic Rhinitis

• Kim HJ
• Kim JH
• Han SA
• Kim W

• KMID: 2536532
• DOI: http://doi.org/10.21053/ceo.2021.01928

Abstract

Objectives
. Host–microbial commensalism can shape the innate immune response in the nasal mucosa, and the microbial characteristics of nasal mucus directly impact the mechanisms of the initial allergic responses in the nasal epithelium. We sought to determine alterations of the microbial composition in the nasal mucus of patients with allergic rhinitis (AR) and to elucidate the interplay between dysbiosis of the nasal microbiome and allergic inflammation.
Methods
. In total, 364,923 high-quality bacterial 16S ribosomal RNA-encoding gene sequence reads from 104 middle turbinate mucosa samples from healthy participants and patients with AR were obtained and analyzed using the Quantitative Insights into Microbial Ecology pipeline.
Results
. We analyzed the microbiota in samples of nasal mucus from patients with AR (n=42) and clinically healthy participants (n=30). The Proteobacteria (Ralstonia genus) and Actinobacteria (Propionibacterium genus) phyla were predominant in the nasal mucus of healthy subjects, whereas the Firmicutes (Staphylococcus genus) phylum was significantly abundant in the nasal mucus of patients with AR. In particular, the Ralstonia genus was significantly dominant in the clinically healthy subjects. Additional pyrosequencing data from 32 subjects (healthy participants: n=15, AR patients: n=17) revealed a greater abundance of Staphylococcus epidermidis, Corynebacterium accolens, and Nocardia coeliaca, accounting for 41.55% of mapped sequences in the nasal mucus of healthy participants. Dysbiosis of the nasal microbiome was more pronounced in patients with AR, and Staphylococcus aureus exhibited the greatest abundance (37.69%) in their nasal mucus, in association with a positive response to house dust mites and patients’ age and height.
Conclusion
. This study revealed alterations in the nasal microbiome in the nasal mucus of patients with AR at the levels of microbial genera and species. S. aureus-dominant dysbiosis was distinctive in the nasal mucus of patients with AR, suggesting a role of host-microbial commensalism in allergic inflammation.

Keyword

Allergic Rhinitis; Nasal Mucosa; Dysbiosis; Microbiota; Species

Figure

• 

  Fig. 1. Alpha-diversity and relative abundance of bacterial phyla and genera. (A) Alpha-diversity richness (P<0.001) and the Shannon index (P=0.39) among observed species. The values were obtained by the non-parametric Wilcoxon test. (B) The Y-axis of the bar graph means the relative abundance of genera of each subject. The X-axis represents each subject from the healthy participants (n=30) and allergic rhinitis (AR) patients (n=42). Only taxa with an average abundance of at least 1% are shown.

• 

  Fig. 2. Difference in bacterial abundance in the middle turbinate between healthy individuals and patients with allergic rhinitis (AR) using the non-parametric Wilcoxon test. The relative abundance of (A) Ralstonia species (spp.), (B) unclassified_Enterobaceriaceae, (C) Lactococcus spp., (D) Staphylococcus spp., and (E) Propionibacterium spp. was compared. **P<0.01, ***P<0.001.

• 

  Fig. 3. Overview of the bacterial taxa, showing differences between healthy individuals and patients with allergic rhinitis (AR). (A) Linear mixed-effects model (LMEM) for comparing healthy participants and patients with AR. The data shown correspond to patients with AR compared to healthy individuals. Upregulation (not shown), downregulation (blue), and no significance (NS; gray). (B) Non-metric multidimensional scaling (NMDS) of bacterial community samples using Bray–Curtis distances. Four genera (Ralstonia, Propionibacterium, Enterobacter, Enterobacteriaceae, and Staphylococcus) with the strongest contribution to sample dissimilarity were revealed by biplot analysis. The Corynebacterium genus was disproportionately represented in patients with AR. (C-E) The correlations between the Ralstonia, Staphylococcus, and Propionibacterium genera were determined by Spearman correlation analysis. spp., species.

• 

  Fig. 4. Composition of microbial species in the nasal mucus of healthy participants and patients with allergic rhinitis (AR). (A) Microbial phyla from middle turbinate mucus of healthy participants (n=15) and patients with AR (n=17) were identified via 16S rRNA gene sequencing. (B) Microbial species from nasal mucus of healthy participants and patients with AR. The distribution of the 126 identified bacterial species is presented in the graph, and the bar graph presents the relative species abundance of the nasal commensal organisms of 17 patients with AR. (C) The distribution of microbial species in the nasal mucus of AR. The bar graph presents the relative species-level abundance of nasal commensal organisms of 17 patients with AR, and the distribution of Staphylococcus epidermidis and S. aureus in each patient is described (red circle: house dust mite [HDM]-positive AR patients). (D) The proportion of Staphylococcus aureus in the nasal mucus from the middle turbinate of each AR patient (n=17) was compared depending on the positive response to HDM (Dermatophagoides pteronyssinus/Dermatophagoides farina).

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