Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota

Abstract

ABSTRACT The tongue dorsum is colonized by a stable microbiota, mostly comprising common commensal taxa. However, the predominance of each taxon varies among individuals. We hypothesized that equilibrium in the tongue microbiota is affected by exposure to butyrate in the oral fluid, which is reported to affect the growth of specific microorganisms. In this study, the bacterial composition of the tongue microbiotas of 69 male adults was determined via 16S rRNA gene sequencing to investigate its relationship to n-butyric acid concentration in oral rinse samples. The tongue microbiotas of individuals with a higher n-butyric acid level had higher relative abundances of Prevotella histicola, Veillonella atypica, and Streptococcus parasanguinis and lower relative abundances of Neisseria subflava and Porphyromonas pasteri. Subsequently, tongue microbiota samples collected from 12 adults were cultivated for 13 h in basal medium containing mucin and different concentrations of sodium butyrate (0, 0.8, 1.6, and 3.2 mM) to assess its effect on the growth of tongue microbiota organisms. The bacterial composition of the cultivated tongue microbiotas also demonstrated a significant gradual shift with an increase in sodium butyrate levels in beta-diversity analysis. N. subflava was significantly less predominant in the microbiota after cultivation with an increased addition of sodium butyrate, although no statistical difference was observed in the other aforementioned taxa. These results suggest that butyrate in the oral fluid is partially involved in the dysbiotic shift of the tongue microbiota. IMPORTANCE Oral microbial populations that are always ingested with saliva have attracted increasing attention because more oral microorganisms than previously known reach distal organs, such as the lungs and intestinal tract, thereby affecting our health. However, although such organisms are predominately derived from the tongue dorsum, the dynamics and determinants of the tongue microbiota composition remain unclear. This study demonstrated that exposure to butyrate could lead to a dysbiotic shift in the tongue microbiota using an observational epidemiological and microbiota cultivation approach. This result adds a new dimension to tongue microbiota ecology.

Keywords

• butyric acid
• tongue microbiota
• 16S rRNA