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...
Main Authors: | , , , , , , , , , |
---|---|
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 |
_version_ | 1811217228143525888 |
---|---|
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. |
first_indexed | 2024-04-12T06:50:54Z |
format | Article |
id | doaj.art-b5893832644f44d892b91b705d039300 |
institution | Directory Open Access Journal |
issn | 2000-2297 |
language | English |
last_indexed | 2024-04-12T06:50:54Z |
publishDate | 2022-12-01 |
publisher | Taylor & Francis Group |
record_format | Article |
series | Journal of Oral Microbiology |
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 |
work_keys_str_mv | AT kyokoyamazaki dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT eijimiyauchi dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT tamotsukato dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT keisukesato dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT watarusuda dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT takahirotsuzuno dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT mikiyamadahara dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT nobuosasaki dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT hiroshiohno dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice AT kazuhisayamazaki dysbiotichumanoralmicrobiotaalterssystemicmetabolismviamodulationofgutmicrobiotaingermfreemice |