The Effects of Smoking on Human Pharynx Microbiota Composition and Stability

Microbiol Spectr. 2023 Feb 14;11(2):e0216621. doi: 10.1128/spectrum.02166-21. Online ahead of print.

Abstract

The oral microbiota is essential to the health of the host, yet little is known about how it responds to disturbances. We examined the oropharyngeal microbiota of 30 individuals over 40 weeks. As the oropharynx is an important gateway to pathogens, and as smoking is associated with increased incidence and severity of respiratory infections, we compared the microbiota of smokers and nonsmokers to shed light on its potential for facilitating infections. We hypothesized that decreased species diversity, decreased community stability, or increased differences in community structure could facilitate invading pathogens. We found that smoking is associated with reduced alpha diversity, greater differences in community structure, and increased environmental filtering. The effects of short-term perturbations (antibiotic use and participants exhibiting cold symptoms) were also investigated. Antibiotic use had a negative effect on alpha diversity, irrespective of smoking status, and both antibiotic use and cold symptoms were associated with highly unique bacterial communities. A stability analysis of models built from the data indicated that there were no differences in local or global stability in the microbial communities of smokers, compared to nonsmokers, and that their microbiota are equally resistant to species invasions. Results from these models suggest that smoker microbiota are perturbed but characterized by alternative stable states that are as stable and invasion-resistant as are the microbiota of nonsmokers. Smoking is unlikely to increase the risk of infectious disease through the altered composition and ecological function of the microbiota; this is more likely due to the effects of smoking on the local and systemic immune system. IMPORTANCE Smoking is associated with an increased risk of respiratory infections. Hypothetically, the altered community diversity of smokers' pharyngeal microbiota, together with changes in their ecological stability properties, could facilitate their invasion by pathogens. To address this question, we analyzed longitudinal microbiota data of baseline healthy individuals who were either smokers or nonsmokers. While the results indicate reduced biodiversity and increased species turnover in the smokers' pharyngeal microbiota, their ecological stability properties were not different from those of the microbiota of nonsmokers, implying, in ecological terms, that the smokers' microbial communities are not less resistant to invasions. Therefore, the study suggests that the increased propensity of respiratory infections that is seen in smokers is more likely associated with changes in the local and systemic immune system than with ecological changes in the microbial communities.

Keywords: antibiotics; cold; community stability; invasion; microbiome; microbiota; oropharynx; perturbation; smoking; stability.