Revealing oral microbiota composition and functionality associated with heavy cigarette smoking

Abstract

Background: Heavy tobacco smoking, a hallmark feature of lung cancer, is drastically predominant in Middle Eastern populations. The precise links between nicotine dependence and the functional contribution of the oral microbiota remain unknown in these populations.

Methods: We evaluated the composition and functional capabilities of oral microbiota with relation to cigarette smoking in 105 adults through shotgun metagenomics using buccal swabs.

Results: The oral microbiota composition in our study subjects was dominated by the phyla Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes, in addition to the genera Prevotella and Veillonella, similar to previously described westernized cohorts. Furthermore, the smoker's oral microbiota represented a significant abundance of Veillonella dispar, Leptotrichia spp. and Prevotella pleuritidis when compared to non-smokers. Within the smoking groups, differential relative abundance testing unveiled relative abundance of Streptobacillus hongkongensis, Fusobacterium massiliense, Prevotella bivia in high nicotine dependent compared to low nicotine dependent profiles based on Fagerström Test for Nicotine Dependence. Functional profiling showed marked differences between smokers and non-smokers. Smokers exhibited an enrichment of Tricarballylate utilization and Lactate racemization when compared to the non-smokers. According to their nicotine dependence, enrichment of Xanthosine utilization, p-Aminobenzoyl-Glutamate utilization, and multidrug efflux pump in Campylobacter jejuni biosynthesis modules were detected in the high nicotine dependent group.

Conclusions: These compositional and functional differences may provide critical insight on how variations in the oral microbiota could predispose to respiratory illnesses and smoke cessation relapse in cigarette smokers. In particular, the observed enrichment of Fusobacterium and Prevotella in the oral microbiota possibly suggests an intriguing linkage to gut and lung cancers.

Keywords: Fagerström test; Nicotine dependence; Oral microbiota; Shotgun metagenomics.

Fig. 1

Differentially abundant taxa between smokers and non-smokers group. Panel shows relative abundance of normalized counts for the top 10 taxa. Results were calculated by negative binomial models (DESEq2 R package) of the form ∼group for differential abundance testing of taxonomic and subsystem level 3 features. P values were calculated with Likelihood Ratio Tests method. All of the above comparison are significant. Smoker and non-smoker corresponding abundance are colored in blue and red, respectively

Fig. 2

Differentially abundant taxa based on FNTD nicotine dependence score. Panel shows relative abundance of normalized counts for the top 10 taxa. Results were calculated by negative binomial models (DESEq2 R package) of the form ∼group for differential abundance testing of taxonomic and subsystem level 3 features. P values were calculated with Likelihood Ratio Tests method. All of the above comparison are significant. Nicotine dependence FTND scores; low, low to moderate, moderate, and high are colored in red, green, blue and pink, respectively

Fig. 3

Differentially abundant gene functions of smokers vs. non-smokers group. Panel shows relative abundance of normalized counts for functional genes using SEED hierarchical categorization. All of the above comparison are significant. Smoker and non-smoker corresponding abundance are colored in blue and red, respectively

Fig. 4

Differentially abundant gene functions based on FNTD nicotine dependence score. Panel shows relative abundance of normalized counts for functional genes using SEED hierarchical categorization. All of the above comparison are significant. Smoking dependence, low, low to moderate, moderate, and high are colored in red, green, blue and pink, respectively