Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome

ABSTRACT Periodontal disease induced by periodontopathic bacteria like Porphyromonas gingivalis is demonstrated to increase the risk of metabolic, inflammatory, and autoimmune disorders. Although precise mechanisms for this connection have not been elucidated, we have proposed mechanisms by which or...

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Autores principales:	Tamotsu Kato, Kyoko Yamazaki, Mayuka Nakajima, Yasuhiro Date, Jun Kikuchi, Koji Hase, Hiroshi Ohno, Kazuhisa Yamazaki
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Porphyromonas gingivalis gut microbiome metabolism periodontitis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0be6d1e12b5442b8bb5eef4a7c0f339d
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spelling	oai:doaj.org-article:0be6d1e12b5442b8bb5eef4a7c0f339d2021-11-15T15:22:26ZOral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome10.1128/mSphere.00460-182379-5042https://doaj.org/article/0be6d1e12b5442b8bb5eef4a7c0f339d2018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00460-18https://doaj.org/toc/2379-5042ABSTRACT Periodontal disease induced by periodontopathic bacteria like Porphyromonas gingivalis is demonstrated to increase the risk of metabolic, inflammatory, and autoimmune disorders. Although precise mechanisms for this connection have not been elucidated, we have proposed mechanisms by which orally administered periodontopathic bacteria might induce changes in gut microbiota composition, barrier function, and immune system, resulting in an increased risk of diseases characterized by low-grade systemic inflammation. Accumulating evidence suggests a profound effect of altered gut metabolite profiles on overall host health. Therefore, it is possible that P. gingivalis can affect these metabolites. To test this, C57BL/6 mice were administered with P. gingivalis W83 orally twice a week for 5 weeks and compared with sham-inoculated mice. The gut microbial communities were analyzed by pyrosequencing the 16S rRNA genes. Inferred metagenomic analysis was used to determine the relative abundance of KEGG pathways encoded in the gut microbiota. Serum metabolites were analyzed using nuclear magnetic resonance (NMR)-based metabolomics coupled with multivariate statistical analyses. Oral administration of P. gingivalis induced a change in gut microbiota composition. The distributions of metabolic pathways differed between the two groups, including those related to amino acid metabolism and, in particular, the genes for phenylalanine, tyrosine, and tryptophan biosynthesis. Also, alanine, glutamine, histidine, tyrosine, and phenylalanine were significantly increased in the serum of P. gingivalis-administered mice. In addition to altering immune modulation and gut barrier function, oral administration of P. gingivalis affects the host’s metabolic profile. This supports our hypothesis regarding a gut-mediated systemic pathology resulting from periodontal disease. IMPORTANCE Increasing evidence suggest that alterations of the gut microbiome underlie metabolic disease pathology by modulating gut metabolite profiles. We have shown that orally administered Porphyromonas gingivalis, a representative periodontopathic bacterium, alters the gut microbiome; that may be a novel mechanism by which periodontitis increases the risk of various diseases. Given the association between periodontal disease and metabolic diseases, it is possible that P. gingivalis can affect the metabolites. Metabolite profiling analysis demonstrated that several amino acids related to a risk of developing diabetes and obesity were elevated in P. gingivalis-administered mice. Our results revealed that the increased risk of various diseases by P. gingivalis might be mediated at least in part by alteration of metabolic profiles. The findings should add new insights into potential links between periodontal disease and systemic disease for investigators in periodontal disease and also for investigators in the field of other diseases, such as metabolic diseases.Tamotsu KatoKyoko YamazakiMayuka NakajimaYasuhiro DateJun KikuchiKoji HaseHiroshi OhnoKazuhisa YamazakiAmerican Society for MicrobiologyarticlePorphyromonas gingivalisgut microbiomemetabolismperiodontitisMicrobiologyQR1-502ENmSphere, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Porphyromonas gingivalis gut microbiome metabolism periodontitis Microbiology QR1-502
spellingShingle	Porphyromonas gingivalis gut microbiome metabolism periodontitis Microbiology QR1-502 Tamotsu Kato Kyoko Yamazaki Mayuka Nakajima Yasuhiro Date Jun Kikuchi Koji Hase Hiroshi Ohno Kazuhisa Yamazaki Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
description	ABSTRACT Periodontal disease induced by periodontopathic bacteria like Porphyromonas gingivalis is demonstrated to increase the risk of metabolic, inflammatory, and autoimmune disorders. Although precise mechanisms for this connection have not been elucidated, we have proposed mechanisms by which orally administered periodontopathic bacteria might induce changes in gut microbiota composition, barrier function, and immune system, resulting in an increased risk of diseases characterized by low-grade systemic inflammation. Accumulating evidence suggests a profound effect of altered gut metabolite profiles on overall host health. Therefore, it is possible that P. gingivalis can affect these metabolites. To test this, C57BL/6 mice were administered with P. gingivalis W83 orally twice a week for 5 weeks and compared with sham-inoculated mice. The gut microbial communities were analyzed by pyrosequencing the 16S rRNA genes. Inferred metagenomic analysis was used to determine the relative abundance of KEGG pathways encoded in the gut microbiota. Serum metabolites were analyzed using nuclear magnetic resonance (NMR)-based metabolomics coupled with multivariate statistical analyses. Oral administration of P. gingivalis induced a change in gut microbiota composition. The distributions of metabolic pathways differed between the two groups, including those related to amino acid metabolism and, in particular, the genes for phenylalanine, tyrosine, and tryptophan biosynthesis. Also, alanine, glutamine, histidine, tyrosine, and phenylalanine were significantly increased in the serum of P. gingivalis-administered mice. In addition to altering immune modulation and gut barrier function, oral administration of P. gingivalis affects the host’s metabolic profile. This supports our hypothesis regarding a gut-mediated systemic pathology resulting from periodontal disease. IMPORTANCE Increasing evidence suggest that alterations of the gut microbiome underlie metabolic disease pathology by modulating gut metabolite profiles. We have shown that orally administered Porphyromonas gingivalis, a representative periodontopathic bacterium, alters the gut microbiome; that may be a novel mechanism by which periodontitis increases the risk of various diseases. Given the association between periodontal disease and metabolic diseases, it is possible that P. gingivalis can affect the metabolites. Metabolite profiling analysis demonstrated that several amino acids related to a risk of developing diabetes and obesity were elevated in P. gingivalis-administered mice. Our results revealed that the increased risk of various diseases by P. gingivalis might be mediated at least in part by alteration of metabolic profiles. The findings should add new insights into potential links between periodontal disease and systemic disease for investigators in periodontal disease and also for investigators in the field of other diseases, such as metabolic diseases.
format	article
author	Tamotsu Kato Kyoko Yamazaki Mayuka Nakajima Yasuhiro Date Jun Kikuchi Koji Hase Hiroshi Ohno Kazuhisa Yamazaki
author_facet	Tamotsu Kato Kyoko Yamazaki Mayuka Nakajima Yasuhiro Date Jun Kikuchi Koji Hase Hiroshi Ohno Kazuhisa Yamazaki
author_sort	Tamotsu Kato
title	Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
title_short	Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
title_full	Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
title_fullStr	Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
title_full_unstemmed	Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome
title_sort	oral administration of <named-content content-type="genus-species">porphyromonas gingivalis</named-content> alters the gut microbiome and serum metabolome
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/0be6d1e12b5442b8bb5eef4a7c0f339d
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Oral Administration of <named-content content-type="genus-species">Porphyromonas gingivalis</named-content> Alters the Gut Microbiome and Serum Metabolome

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