The Role of Indoor Microbiome and Metabolites in Shaping Children’s Nasal and Oral Microbiota: A Pilot Multi-Omic Analysis

Abstract

Maintaining a diverse and well-balanced nasal and oral microbiota is vital for human health. However, the impact of indoor microbiome and metabolites on nasal and oral microbiota remains largely unknown. Fifty-six children in Shanghai were surveyed to complete a questionnaire about their personal and environmental characteristics. The indoor microbiome and metabolites from vacuumed indoor dust were profiled via shotgun metagenomics and untargeted liquid chromatography-mass spectrometry (LC–MS). The nasal and oral microbiota in children was characterized using full-length 16S rRNA sequencing from PacBio. Associations between personal/environmental characteristics and the nasal/oral microbiota were calculated using PERMANOVA and regression analyses. We identified 6247, 431, and 342 microbial species in the indoor dust, nasal, and oral cavities, respectively. The overall nasal and oral microbial composition showed significant associations with environmental tobacco smoke (ETS) exposure during pregnancy and early childhood (p = 0.005 and 0.03, respectively), and the abundance of total indoor flavonoids and two mycotoxins (deoxynivalenol and nivalenol) (p = 0.01, 0.02, and 0.03, respectively). Notably, the abundance of several flavonoids, such as baicalein, eupatilin, isoliquiritigenin, tangeritin, and hesperidin, showed positive correlations with alpha diversity and the abundance of protective microbial taxa in nasal and oral cavities (p < 0.02), suggesting their potential beneficial roles in promoting nasal/oral health. Conversely, high carbohydrate/fat food intake and ETS exposure diminished protective microorganisms while augmenting risky microorganisms in the nasal/oral cavities. Further, potential microbial transfer was observed from the indoor environment to the childhood oral cavity (Moraxella catarrhalis, Streptococcus mitis, and Streptococcus salivarius), which could potentially increase virulence factors related to adherence and immune modulation and vancomycin resistance genes in children. This is the first study to reveal the association between the indoor microbiome/metabolites and nasal/oral microbiota using multi-omic approaches. These findings reveal potential protective and risk factors related to the indoor microbial environment.

Exploring the role of indoor microbiome and environmental characteristics in rhinitis symptoms among university students

“…A majority of the microbial taxa identified in this study has not been reported in previous indoor microbiome and rhinitis/asthma studies (Fu et al, 2020b;Fu et al, 2022;Fu et al, 2023a;Sun et al, 2023;Zhang et al, 2023b). Several reasons could underlie this discrepancy.…”

The Third-Generation Sequencing Challenge: Novel Insights for the Omic Sciences

“…Another comparative analysis revealed that the low sequencing accuracy of PacBio may impair its taxonomic resolution in the study of human gut microbiota [88]. Nevertheless, PacBio sequencing has been successfully used in several metagenomic studies and was able, for example, to identify the microbiome profiles of heavy-metal-contaminated soils [89], analyze extrachromosomal genetic elements (mainly plasmids) in the human gut [90], characterize the airway microbiome of chronic obstructive pulmonary disease patients [91], identify low-biomass human gut phageomes [92], and highlight the association between the indoor microbiome and nasal/oral humans microbiome [93]. A very recent paper by Eisenhofer and colleagues compared shotgun metagenomics carried out with both NGS and PacBio technologies and found that even if PacBio ameliorates the quality of bacterial genome assembly, it is more expensive and needs a higher sequencing coverage with respect to short reads, thus suggesting that the most optimal strategy depends on the aims of each specific project [94].…”