Potential of Prebiotic D-Tagatose for Prevention of Oral Disease

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 t...

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Autores principales:	Shota Mayumi, Masae Kuboniwa, Akito Sakanaka, Ei Hashino, Asuka Ishikawa, Yura Ijima, Atsuo Amano
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	d-tagatose biofilm transcriptomics metabolomics (OMICS) Streptococcus mutans (S. mutans) Streptococcus gordonii Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ede21ba8fd784606beb1e7eb1c868285
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spelling	oai:doaj.org-article:ede21ba8fd784606beb1e7eb1c8682852021-11-05T14:45:13ZPotential of Prebiotic D-Tagatose for Prevention of Oral Disease2235-298810.3389/fcimb.2021.767944https://doaj.org/article/ede21ba8fd784606beb1e7eb1c8682852021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fcimb.2021.767944/fullhttps://doaj.org/toc/2235-2988Recent 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.Shota MayumiMasae KuboniwaAkito SakanakaEi HashinoAsuka IshikawaYura IjimaAtsuo AmanoFrontiers Media S.A.articled-tagatosebiofilmtranscriptomicsmetabolomics (OMICS)Streptococcus mutans (S. mutans)Streptococcus gordoniiMicrobiologyQR1-502ENFrontiers in Cellular and Infection Microbiology, Vol 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	d-tagatose biofilm transcriptomics metabolomics (OMICS) Streptococcus mutans (S. mutans) Streptococcus gordonii Microbiology QR1-502
spellingShingle	d-tagatose biofilm transcriptomics metabolomics (OMICS) Streptococcus mutans (S. mutans) Streptococcus gordonii Microbiology QR1-502 Shota Mayumi Masae Kuboniwa Akito Sakanaka Ei Hashino Asuka Ishikawa Yura Ijima Atsuo Amano Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
description	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.
format	article
author	Shota Mayumi Masae Kuboniwa Akito Sakanaka Ei Hashino Asuka Ishikawa Yura Ijima Atsuo Amano
author_facet	Shota Mayumi Masae Kuboniwa Akito Sakanaka Ei Hashino Asuka Ishikawa Yura Ijima Atsuo Amano
author_sort	Shota Mayumi
title	Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
title_short	Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
title_full	Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
title_fullStr	Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
title_full_unstemmed	Potential of Prebiotic D-Tagatose for Prevention of Oral Disease
title_sort	potential of prebiotic d-tagatose for prevention of oral disease
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/ede21ba8fd784606beb1e7eb1c868285
work_keys_str_mv	AT shotamayumi potentialofprebioticdtagatoseforpreventionoforaldisease AT masaekuboniwa potentialofprebioticdtagatoseforpreventionoforaldisease AT akitosakanaka potentialofprebioticdtagatoseforpreventionoforaldisease AT eihashino potentialofprebioticdtagatoseforpreventionoforaldisease AT asukaishikawa potentialofprebioticdtagatoseforpreventionoforaldisease AT yuraijima potentialofprebioticdtagatoseforpreventionoforaldisease AT atsuoamano potentialofprebioticdtagatoseforpreventionoforaldisease
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Potential of Prebiotic D-Tagatose for Prevention of Oral Disease

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