Abstract
BackgroundDental plaque is composed of hundreds of bacterial taxonomic units and represents one of the most diverse and stable microbial ecosystems associated with the human body. Taxonomic composition and functional capacity of mature plaque is gradually shaped during several stages of community assembly via processes such as co-aggregation, competition for space and resources, and by bacterially produced reactive agents. Knowledge on the dynamics of assembly within complex communities is very limited and derives mainly from studies composed of a limited number of bacterial species. To fill current knowledge gaps, we applied parallel metagenomic and metatranscriptomic analyses during assembly and maturation of an in vitro oral biofilm. This model system has previously demonstrated remarkable reproducibility in taxonomic composition across replicate samples during maturation.ResultsTime course analysis of the biofilm maturation was performed by parallel sampling every 2–3 h for 24 h for both DNA and RNA. Metagenomic analyses revealed that community taxonomy changed most dramatically between three and six hours of growth when pH dropped from 6.5 to 5.5. By applying comparative metatranscriptome analysis we could identify major shifts in overall community activities between six and nine hours of growth when pH dropped below 5.5, as 29,015 genes were significantly up- or down- expressed. Several of the differentially expressed genes showed unique activities for individual bacterial genomes and were associated with pyruvate and lactate metabolism, two-component signaling pathways, production of antibacterial molecules, iron sequestration, pH neutralization, protein hydrolysis, and surface attachment. Our analysis also revealed several mechanisms responsible for the niche expansion of the cariogenic pathogen Lactobacillus fermentum.ConclusionIt is highly regarded that acidic conditions in dental plaque cause a net loss of enamel from teeth. Here, as pH drops below 5.5 pH to 4.7, we observe blooms of cariogenic lactobacilli, and a transition point of many bacterial gene expression activities within the community. To our knowledge, this represents the first study of the assembly and maturation of a complex oral bacterial biofilm community that addresses gene level functional responses over time.
Highlights
Dental plaque is composed of hundreds of bacterial taxonomic units and represents one of the most diverse and stable microbial ecosystems associated with the human body
In line with our previous oral in vitro biofilm studies [25,26,27], saliva was chosen as inoculum for this model since the initial binding and subsequent biofilm assembly on a tooth surface is initiated by early colonizing bacteria found in saliva, which bind to the newly deposited acquired pellicle containing host components [35]
The cariogenic and lactic acid producing L. fermentum increased in relative abundance both at the Messenger ribonucleic acid (mRNA) and Deoxyribonucleic acid (DNA) levels at later time points, which suggests its role as a secondary colonizer
Summary
Dental plaque is composed of hundreds of bacterial taxonomic units and represents one of the most diverse and stable microbial ecosystems associated with the human body. Understanding the processes underlying the assembly of complex oral biofilm communities is of high importance for maintaining a healthy microbiome composition and learning how dysbiosis occurs Oral bacteria and their metabolites can interact directly with human host cells, both as protective barriers against pathogen invasion [2], and as causative agents of oral diseases [3, 4] (e.g. caries and periodontal disease), as well as systemic diseases (e.g. type-2 diabetes and cardiovascular disease) [5, 6]. Major signatures of oral streptococci include the consumption of carbohydrates and the rapid secretion of L-lactate and hydrogen peroxide (H2O2), that can accumulate to high (millimolar) concentrations within mixed-species biofilms [14] These capacities render streptococci extremely competitive by respectively limiting carbon source availability, and causing oxidative stress to surrounding microbes. A known example of such organisms are bacteria belonging to the Veillonella genus, which carry H2O2 resistance genes [15], and can utilize L-lactate as a sole carbon source [16]
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