Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice

Background The effect of oral microbiota on the intestinal microbiota has garnered growing attention as a mechanism linking periodontal diseases to systemic diseases. However, the salivary microbiota is diverse and comprises numerous bacteria with a largely similar composition in healthy individuals...

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Main Authors: Kyoko Yamazaki, Eiji Miyauchi, Tamotsu Kato, Keisuke Sato, Wataru Suda, Takahiro Tsuzuno, Miki Yamada-Hara, Nobuo Sasaki, Hiroshi Ohno, Kazuhisa Yamazaki
Format: Article
Language:English
Published: Taylor & Francis Group 2022-12-01
Series:Journal of Oral Microbiology
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/20002297.2022.2110194
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author Kyoko Yamazaki
Eiji Miyauchi
Tamotsu Kato
Keisuke Sato
Wataru Suda
Takahiro Tsuzuno
Miki Yamada-Hara
Nobuo Sasaki
Hiroshi Ohno
Kazuhisa Yamazaki
author_facet Kyoko Yamazaki
Eiji Miyauchi
Tamotsu Kato
Keisuke Sato
Wataru Suda
Takahiro Tsuzuno
Miki Yamada-Hara
Nobuo Sasaki
Hiroshi Ohno
Kazuhisa Yamazaki
author_sort Kyoko Yamazaki
collection DOAJ
description Background The effect of oral microbiota on the intestinal microbiota has garnered growing attention as a mechanism linking periodontal diseases to systemic diseases. However, the salivary microbiota is diverse and comprises numerous bacteria with a largely similar composition in healthy individuals and periodontitis patients.Aim We explored how health-associated and periodontitis-associated salivary microbiota differently colonized the intestine and their subsequent systemic effects.Methods The salivary microbiota was collected from a healthy individual and a periodontitis patient and gavaged into C57BL/6NJcl[GF] mice. Gut microbial communities, hepatic gene expression profiles, and serum metabolites were analyzed.Results The gut microbial composition was significantly different between periodontitis-associated microbiota-administered (PAO) and health-associated oral microbiota-administered (HAO) mice. The hepatic gene expression profile demonstrated a distinct pattern between the two groups, with higher expression of lipid and glucose metabolism-related genes. Disease-associated metabolites such as 2-hydroxyisobutyric acid and hydroxybenzoic acid were elevated in PAO mice. These metabolites were significantly correlated with characteristic gut microbial taxa in PAO mice. Conversely, health-associated oral microbiota were associated with higher levels of beneficial serum metabolites in HAO mice.Conclusion The multi-omics approach used in this study revealed that periodontitis-associated oral microbiota is associated with the induction of disease phenotype when they colonized the gut of germ-free mice.
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spelling doaj.art-b5893832644f44d892b91b705d0393002022-12-22T03:43:21ZengTaylor & Francis GroupJournal of Oral Microbiology2000-22972022-12-0114110.1080/20002297.2022.2110194Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free miceKyoko Yamazaki0Eiji Miyauchi1Tamotsu Kato2Keisuke Sato3Wataru Suda4Takahiro Tsuzuno5Miki Yamada-Hara6Nobuo Sasaki7Hiroshi Ohno8Kazuhisa Yamazaki9Division of Periodontology, Niigata University Graduate School of Medical and Dental Sciences, Niigata JapanLaboratory for Intestinal Ecosystem, RIKEN Centre for Integrative Medical Sciences (IMS), Kanagawa JapanLaboratory for Intestinal Ecosystem, RIKEN Centre for Integrative Medical Sciences (IMS), Kanagawa JapanDivision of Periodontology, Niigata University Graduate School of Medical and Dental Sciences, Niigata JapanLaboratory for Microbiome Sciences, RIKEN Center for Integrative Medical Sciences, Yokohama, JapanDivision of Periodontology, Niigata University Graduate School of Medical and Dental Sciences, Niigata JapanDivision of Periodontology, Niigata University Graduate School of Medical and Dental Sciences, Niigata JapanLaboratory of Mucosal Ecosystem Design, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi, Gunma JapanLaboratory for Intestinal Ecosystem, RIKEN Centre for Integrative Medical Sciences (IMS), Kanagawa JapanLaboratory for Intestinal Ecosystem, RIKEN Centre for Integrative Medical Sciences (IMS), Kanagawa JapanBackground The effect of oral microbiota on the intestinal microbiota has garnered growing attention as a mechanism linking periodontal diseases to systemic diseases. However, the salivary microbiota is diverse and comprises numerous bacteria with a largely similar composition in healthy individuals and periodontitis patients.Aim We explored how health-associated and periodontitis-associated salivary microbiota differently colonized the intestine and their subsequent systemic effects.Methods The salivary microbiota was collected from a healthy individual and a periodontitis patient and gavaged into C57BL/6NJcl[GF] mice. Gut microbial communities, hepatic gene expression profiles, and serum metabolites were analyzed.Results The gut microbial composition was significantly different between periodontitis-associated microbiota-administered (PAO) and health-associated oral microbiota-administered (HAO) mice. The hepatic gene expression profile demonstrated a distinct pattern between the two groups, with higher expression of lipid and glucose metabolism-related genes. Disease-associated metabolites such as 2-hydroxyisobutyric acid and hydroxybenzoic acid were elevated in PAO mice. These metabolites were significantly correlated with characteristic gut microbial taxa in PAO mice. Conversely, health-associated oral microbiota were associated with higher levels of beneficial serum metabolites in HAO mice.Conclusion The multi-omics approach used in this study revealed that periodontitis-associated oral microbiota is associated with the induction of disease phenotype when they colonized the gut of germ-free mice.https://www.tandfonline.com/doi/10.1080/20002297.2022.2110194Oralgutmicrobiomelivertranscriptomemetabolome
spellingShingle Kyoko Yamazaki
Eiji Miyauchi
Tamotsu Kato
Keisuke Sato
Wataru Suda
Takahiro Tsuzuno
Miki Yamada-Hara
Nobuo Sasaki
Hiroshi Ohno
Kazuhisa Yamazaki
Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
Journal of Oral Microbiology
Oral
gut
microbiome
liver
transcriptome
metabolome
title Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
title_full Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
title_fullStr Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
title_full_unstemmed Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
title_short Dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ-free mice
title_sort dysbiotic human oral microbiota alters systemic metabolism via modulation of gut microbiota in germ free mice
topic Oral
gut
microbiome
liver
transcriptome
metabolome
url https://www.tandfonline.com/doi/10.1080/20002297.2022.2110194
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