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

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 affe...

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Autores principales: Chen, Bou-Jon, Takeshita, Toru, Tajikara, Teppei, Asakawa, Mikari, Kageyama, Shinya, Shibata, Yukie, Ayukawa, Yasunori, Yano, Yoshitaka, Yamashita, Yoshihisa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942584/
https://www.ncbi.nlm.nih.gov/pubmed/36507724
http://dx.doi.org/10.1128/msphere.00490-22
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author Chen, Bou-Jon
Takeshita, Toru
Tajikara, Teppei
Asakawa, Mikari
Kageyama, Shinya
Shibata, Yukie
Ayukawa, Yasunori
Yano, Yoshitaka
Yamashita, Yoshihisa
author_facet Chen, Bou-Jon
Takeshita, Toru
Tajikara, Teppei
Asakawa, Mikari
Kageyama, Shinya
Shibata, Yukie
Ayukawa, Yasunori
Yano, Yoshitaka
Yamashita, Yoshihisa
author_sort Chen, Bou-Jon
collection PubMed
description 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.
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spelling pubmed-99425842023-02-22 Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota Chen, Bou-Jon Takeshita, Toru Tajikara, Teppei Asakawa, Mikari Kageyama, Shinya Shibata, Yukie Ayukawa, Yasunori Yano, Yoshitaka Yamashita, Yoshihisa mSphere Research Article 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. American Society for Microbiology 2022-12-12 /pmc/articles/PMC9942584/ /pubmed/36507724 http://dx.doi.org/10.1128/msphere.00490-22 Text en Copyright © 2022 Chen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Chen, Bou-Jon
Takeshita, Toru
Tajikara, Teppei
Asakawa, Mikari
Kageyama, Shinya
Shibata, Yukie
Ayukawa, Yasunori
Yano, Yoshitaka
Yamashita, Yoshihisa
Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title_full Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title_fullStr Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title_full_unstemmed Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title_short Butyrate as a Potential Driver of a Dysbiotic Shift of the Tongue Microbiota
title_sort butyrate as a potential driver of a dysbiotic shift of the tongue microbiota
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942584/
https://www.ncbi.nlm.nih.gov/pubmed/36507724
http://dx.doi.org/10.1128/msphere.00490-22
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