Abstract
Cigarette smokers have an increased risk of infectious diseases involving the respiratory tract. Some effects of smoking on specific respiratory tract bacteria have been described, but the consequences for global airway microbial community composition have not been determined. Here, we used culture-independent high-density sequencing to analyze the microbiota from the right and left nasopharynx and oropharynx of 29 smoking and 33 nonsmoking healthy asymptomatic adults to assess microbial composition and effects of cigarette smoking. Bacterial communities were profiled using 454 pyrosequencing of 16S sequence tags (803,391 total reads), aligned to 16S rRNA databases, and communities compared using the UniFrac distance metric. A Random Forest machine-learning algorithm was used to predict smoking status and identify taxa that best distinguished between smokers and nonsmokers. Community composition was primarily determined by airway site, with individuals exhibiting minimal side-of-body or temporal variation. Within airway habitats, microbiota from smokers were significantly more diverse than nonsmokers and clustered separately. The distributions of several genera were systematically altered by smoking in both the oro- and nasopharynx, and there was an enrichment of anaerobic lineages associated with periodontal disease in the oropharynx. These results indicate that distinct regions of the human upper respiratory tract contain characteristic microbial communities that exhibit disordered patterns in cigarette smokers, both in individual components and global structure, which may contribute to the prevalence of respiratory tract complications in this population.
Highlights
One in five adults currently smoke cigarettes in the U.S.A
The upper airway serves as a site both for local upper respiratory tract infections, and for colonization by pathogenic microorganisms that can result in subsequent lower respiratory tract infection or invasive disease
We present the first comprehensive analysis of upper airway bacterial colonization in healthy adult cigarette smokers compared with nonsmokers using deep sequencing of microbial 16S rRNA genes
Summary
One in five adults currently smoke cigarettes in the U.S.A. (www.cdc.gov/tobacco). Previous reports using limited culture-based methods have linked exposure to cigarette smoke with altered upper airway microbial colonization. Both active smoking in adults and passive exposure to cigarette smoke in children is associated with increased carriage of pathogenic organisms in the upper airways [3]. Cigarette smoke extract differentially effects the survival of specific microbial species isolated from the human oral cavity, selecting for growth of gram negative bacteria such as Pseudomonas aeruginosa and Klebsiella spp. Cigarettes themselves harbor a broad range of potential pathogens, including Acinetobacter, Bacillus, Burkholderia, Clostridium, Klebsiella, Pseudomonas aeruginosa, and Serratia lineages [9] and may be a direct source of exposure to diseasecausing organisms
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