Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Hara, Takeshi; Sakanaka, Akito; Lamont, Richard J.; Amano, Atsuo; Kuboniwa, Masae; Das, Promi

doi:https://doi.org/10.1128/msystems.00764-23

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Hara, Takeshi; Sakanaka, Akito; Lamont, Richard J. et al.

mSystems, 2024, 2, 118

Number of Access:686（2025-07-26 08:40 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/94593

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Title	Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production
Creator	NRID 1000010898224 1000010898224 ORCID 0000-0002-7689-2995 0000-0002-7689-2995 researchmap permalink md-10726-th md-10726-th CreatorName Hara, Takeshi
	NRID 1000090815557 1000090815557 researchmap permalink sknk1022 sknk1022 Scopus Author ID 56814868300 56814868300 ORCID 0000-0001-9733-6886 0000-0001-9733-6886 CreatorName Sakanaka, Akito
	CreatorName Lamont, Richard J.
	NRID 1000050193024 1000050193024 researchmap permalink read0014208 read0014208 Scopus Author ID 7101649822 7101649822 CreatorName Amano, Atsuo
	NRID 1000000303983 1000000303983 ORCID 0000-0002-3332-2431 0000-0002-3332-2431 researchmap permalink MasaeKuboniwa_URL MasaeKuboniwa_URL Scopus Author ID 56089471500 56089471500 CreatorName Kuboniwa, Masae
	CreatorName Das, Promi
Description	Hara Takeshi, Sakanaka Akito, Lamont Richard J., et al. Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production. mSystems 2, 118 (2024); https://doi.org/10.1128/msystems.00764-23.
Abstract	The major oral odor compound methyl mercaptan (CH3SH) is strongly associated with halitosis and periodontitis. CH3SH production stems from the metabolism of polymicrobial communities in periodontal pockets and on the tongue dorsum. However, understanding of CH3SH-producing oral bacteria and their interactions is limited. This study aimed to investigate CH3SH production by major oral bacteria and the impact of interspecies interactions on its generation. Using a newly constructed large-volume anaerobic noncontact coculture system, Fusobacterium nucleatum was found to be a potent producer of CH3SH, with that production stimulated by metabolic interactions with Streptococcus gordonii, an early dental plaque colonizer. Furthermore, analysis of extracellular amino acids using an S. gordonii arginine-ornithine antiporter (ArcD) mutant demonstrated that ornithine excreted from S. gordonii is a key contributor to increased CH3SH production by F. nucleatum. Further study with 13C, 15N-methionine, as well as gene expression analysis, revealed that ornithine secreted by S. gordonii increased the demand for methionine through accelerated polyamine synthesis by F. nucleatum, leading to elevated methionine pathway activity and CH3SH production. Collectively, these findings suggest that interaction between S. gordonii and F. nucleatum plays a key role in CH3SH production, providing a new insight into the mechanism of CH3SH generation in oral microbial communities. A better understanding of the underlying interactions among oral bacteria involved in CH3SH generation can lead to the development of more appropriate prophylactic approaches to treat halitosis and periodontitis. An intervention approach like selectively disrupting this interspecies network could also offer a powerful therapeutic strategy.
Publisher	American Society for Microbiology
Source Title	mSystems
Volume (Issue)	2
Page	118
Date of Issued	2024-01-30
Language	English
Handle URL	https://hdl.handle.net/11094/94593
eISSN	23795077
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1128/msystems.00764-23
Access Rights	open access
CopyRight	This article is licensed under a Creative Commons Attribution 4.0 International License.
oaire:version	Version of Record
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCMI Type	Text
DCTERMS.bibliographicCitation	mSystems. 2024, 2, p. 118
DC.title	Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production
DC.creator	Hara, Takeshi
	Sakanaka, Akito
	Lamont, Richard J.
	Amano, Atsuo
	Kuboniwa, Masae
	Das, Promi
DC.publisher	American Society for Microbiology
DC.language' scheme='DCTERMS.RFC1766	English
DC.type' scheme='DCTERMS.DCMIType	Text
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2024-01-30
DC.identifier	https://doi.org/10.1128/msystems.00764-23
DC.description	Hara Takeshi, Sakanaka Akito, Lamont Richard J., et al. Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production. mSystems 2, 118 (2024); https://doi.org/10.1128/msystems.00764-23.
DCTERMS.abstract	The major oral odor compound methyl mercaptan (CH3SH) is strongly associated with halitosis and periodontitis. CH3SH production stems from the metabolism of polymicrobial communities in periodontal pockets and on the tongue dorsum. However, understanding of CH3SH-producing oral bacteria and their interactions is limited. This study aimed to investigate CH3SH production by major oral bacteria and the impact of interspecies interactions on its generation. Using a newly constructed large-volume anaerobic noncontact coculture system, Fusobacterium nucleatum was found to be a potent producer of CH3SH, with that production stimulated by metabolic interactions with Streptococcus gordonii, an early dental plaque colonizer. Furthermore, analysis of extracellular amino acids using an S. gordonii arginine-ornithine antiporter (ArcD) mutant demonstrated that ornithine excreted from S. gordonii is a key contributor to increased CH3SH production by F. nucleatum. Further study with 13C, 15N-methionine, as well as gene expression analysis, revealed that ornithine secreted by S. gordonii increased the demand for methionine through accelerated polyamine synthesis by F. nucleatum, leading to elevated methionine pathway activity and CH3SH production. Collectively, these findings suggest that interaction between S. gordonii and F. nucleatum plays a key role in CH3SH production, providing a new insight into the mechanism of CH3SH generation in oral microbial communities. A better understanding of the underlying interactions among oral bacteria involved in CH3SH generation can lead to the development of more appropriate prophylactic approaches to treat halitosis and periodontitis. An intervention approach like selectively disrupting this interspecies network could also offer a powerful therapeutic strategy.
DC.rights	This article is licensed under a Creative Commons Attribution 4.0 International License.
DC.format	94593
citation_title	Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production
citation_author	Hara, Takeshi
	Sakanaka, Akito
	Lamont, Richard J.
	Amano, Atsuo
	Kuboniwa, Masae
	Das, Promi
citation_publisher	American Society for Microbiology
citation_language	English
citation_date	2024-01-30
citation_journal_title	mSystems
citation_volume	2
citation_firstpage	118
citation_doi	https://doi.org/10.1128/msystems.00764-23
citation_public_url	https://hdl.handle.net/11094/94593

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

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