Abstract
Recent studies have shown phenotypic and metabolic heterogeneity in related species including Streptococcus oralis, a typical oral commensal bacterium, Streptococcus mutans, a cariogenic bacterium, and Streptococcus gordonii, which functions as an accessory pathogen in periodontopathic biofilm. In this study, metabolites characteristically contained in the saliva of individuals with good oral hygiene were determined, after which the effects of an identified prebiotic candidate, D-tagatose, on phenotype, gene expression, and metabolic profiles of those three key bacterial species were investigated. Examinations of the saliva metabolome of 18 systemically healthy volunteers identified salivary D-tagatose as associated with lower dental biofilm abundance in the oral cavity (Spearman’s correlation coefficient; r = -0.603, p = 0.008), then the effects of D-tagatose on oral streptococci were analyzed in vitro. In chemically defined medium (CDM) containing D-tagatose as the sole carbohydrate source, S. mutans and S. gordonii each showed negligible biofilm formation, whereas significant biofilms were formed in cultures of S. oralis. Furthermore, even in the presence of glucose, S. mutans and S. gordonii showed growth suppression and decreases in the final viable cell count in a D-tagatose concentration-dependent manner. In contrast, no inhibitory effects of D-tagatose on the growth of S. oralis were observed. To investigate species-specific inhibition by D-tagatose, the metabolomic profiles of D-tagatose-treated S. mutans, S. gordonii, and S. oralis cells were examined. The intracellular amounts of pyruvate-derived amino acids in S. mutans and S. gordonii, but not in S. oralis, such as branched-chain amino acids and alanine, tended to decrease in the presence of D-tagatose. This phenomenon indicates that D-tagatose inhibits growth of those bacteria by affecting glycolysis and its downstream metabolism. In conclusion, the present study provides evidence that D-tagatose is abundant in saliva of individuals with good oral health. Additionally, experimental results demonstrated that D-tagatose selectively inhibits growth of the oral pathogens S. mutans and S. gordonii. In contrast, the oral commensal S. oralis seemed to be negligibly affected, thus highlighting the potential of administration of D-tagatose as an oral prebiotic for its ability to manipulate the metabolism of those targeted oral streptococci.
Highlights
Dental caries and periodontal disease are prevalent polymicrobial infections found in the human oral cavity, which often lead to tooth loss and have effects on general health (Lamont and Hajishengallis, 2015; Johansson et al, 2016; Bernabe et al, 2020)
Five calibrated and licensed dentists evaluated plaque accumulation at four sites per tooth for all present, and the average per tooth was used for the total score, which was defined as modified plaque index (Sakanaka et al, 2017). mPlI was not obtained in that manner for one of the subjects, and all participants except for this subject were asked to expectorate unstimulated whole saliva over a 10-minute period into a 50-mL tube (Corning, Corning, NY, USA) that was kept on ice
Growth of S. gordonii, S. mutans, and S. oralis in BHI containing D-tagatose was examined, which showed that the lag phase of growth of S. gordonii and S. mutans was prolonged in the presence of D-tagatose at a concentration of 0.5% or higher (Figures 2A, 3A)
Summary
Dental caries and periodontal disease are prevalent polymicrobial infections found in the human oral cavity, which often lead to tooth loss and have effects on general health (Lamont and Hajishengallis, 2015; Johansson et al, 2016; Bernabe et al, 2020) Such infections develop when dental biofilm shifts from a symbiotic to dysbiotic state (Lamont et al, 2018) and disruption of biofilm showing symbiosis has been found to be associated with its maturation over time (Mira et al, 2017). On the other hand, during formation of cariogenic biofilm, cariogenic bacteria represented by the major strain Streptococcus mutans become dominant due to multiple factors related to lifestyle and a diet rich in sugars (Selwitz et al, 2007; Gross et al, 2012) In both cases, oral streptococci, which are early colonizers, play a critical role
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