Ecological Perturbations Impact Species-Specific Gene Expression of the Oral Microbiota

Abstract Background: The purpose of the present investigation was to use the oral cavity as an in-vivo model to study the impact of internal and external perturbations on bacterial biofilm communities. We tested the hypotheses that bacterial gene expression of the healthy microbiota reflects habituation to site-specific ecological perturbations, and that the perturbation effect of chronic inflammation, i.e. periodontitis, impacts bacterial gene expression not only locally, but also at other sites of the oral cavity. Oral microbial samples were collected from three oral sites – plaque, tongue and saliva from patients with periodontitis and healthy controls. Paired metagenomics and metatranscriptomics were used to perform concomitant characterization of taxonomic composition and to determine species specific bacterial activity as expressed by the ratio of messenger RNA to the corresponding genomic DNA.Results: Here we show the impact of two perturbations – oral site and periodontitis - on bacterial gene expression of the oral microbiota. The oral site was the main determinant of taxonomic composition as well as bacterial gene expression. However, bacterial activity at the three oral sites (plaque, tongue, and saliva) was significantly impacted by periodontitis, with a reduction of the carbohydrate metabolism.Conclusions: Data from the present study characterize the impact of two perturbations – oral site and periodontitis - on bacterial gene expression of the oral microbiota. The oral site was the main determinant of taxonomic composition as well as bacterial gene expression. However, presence of periodontitis had impact on bacterial activity of both plaque but also on tongue and the salivary microbiota. Collectively, data suggest that periodontitis associates with impaired carbohydrate metabolism of the oral microbiota. Future longitudinal and interventional studies are warranted to evaluate the potential pathogenic role of impaired bacterial carbohydrate metabolism not only in periodontitis, but also in other diseases with low grade inflammation, such as type 2 diabetes mellitus.