The DOI matches its Crossref record, with a small difference in title or year; 65 of the 65 references it cites were found in a registry or an index.
Oral Microbiome Metabolism: From “Who Are They?” to “What Are They Doing?”
Abstract
Recent advances in molecular biology have facilitated analyses of the oral microbiome (“Who are they?”); however, its functions (e.g., metabolic activities) are poorly understood (“What are they doing?”). This review aims to summarize our current understanding of the metabolism of the oral microbiome. Saccharolytic bacteria—including Streptococcus, Actinomyces, and Lactobacillus species—degrade carbohydrates into organic acids via the Embden-Meyerhof-Parnas pathway and several of its branch pathways, resulting in dental caries, while alkalization and acid neutralization via the arginine deiminase system, urease, and so on, counteract acidification. Proteolytic/amino acid–degrading bacteria, including Prevotella and Porphyromonas species, break down proteins and peptides into amino acids and degrade them further via specific pathways to produce short-chain fatty acids, ammonia, sulfur compounds, and indole/skatole, which act as virulent and modifying factors in periodontitis and oral malodor. Furthermore, it is suggested that ethanol-derived acetaldehyde can cause oral cancer, while nitrate-derived nitrite can aid caries prevention and systemic health. Microbial metabolic activity is influenced by the oral environment; however, it can also modify the oral environment, enhance the pathogenicity of bacteria, and induce microbial selection to create more pathogenic microbiome. Taking a metabolomic approach to analyzing the oral microbiome is crucial to improving our understanding of the functions of the oral microbiome.
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In the citing paper
“These bacteria can cause demineralization of dental enamel and development of carious lesions, and on the other hand, promote bacterial acidogenicity and acidification by increasing cell membrane permeability to protons, induction of H+- ATPase activity, and stimulation of metabolic pathways involved in acid neutralization and alkalinization [83].”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“They are broken down into peptides and amino acids (aspartate, serine, and cysteine) through the action of host proteases and peptidases [83].”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“However, the degradation of protein substrates plays an important role in the pathogenesis of the periodontal disease [83].”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“Fermentation of amino acids neutralizes acidic environments, creating a more favorable atmosphere for the growth of other periodontitis’ pathogens [83].”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“Amino acids are fermented to generate short-chain fatty acids, such as propionate, butyrate, succinate, acetate, and formate [83].”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“The increased depth of the gingival pocket and the increased production of gingival crevicular fluid induces an increase in bacteria involved in protein degradation.”
From A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis (2022) · cites this paper as [83]
In the citing paper
“Over 250 species from the oral cavity have been isolated in culture and characterized, including several key pathogens, such as Streptococcus mutans, Porphyromonas gingivalis, Tannerella forsythia, and Aggregatibacter actinomycetemcomitans, involved in the etiology of dental caries and periodontal disease.7, 8, 9”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Moreover, processed carbohydrate consumption has been associated with increased incidence of periodontal disease.8, 24, 26, 181, 188, 251”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Digestion of starch is initiated in the oral cavity through the action of salivary alpha‐amylase that catalyzes the hydrolysis of starch by cleaving α‐1,4‐glycosidic linkages to yield smaller saccharide moieties, such as maltose, maltotriose, and alpha‐limit dextrins,279, 280 which can be utilized by early biofilm colonizers as well as by some periodontal pathogens.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Such processes encourage the outgrowth of acidogenic bacteria, such as S mutans, lactobacilli, and bifidobacteria that enhance the carcinogenicity of dental plaque.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Pathways in which sugar is metabolized are also shared among some periodontal pathogens, such as Fusobacterium and Prevotella, which can likewise cause acidification.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“During the development of periodontal disease, protein‐rich and neutral‐alkaline environmental pressures promote the outgrowth of periodontal pathogens.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Inflammatory processes promote the outgrowth of inflammophilic bacteria via the production of proteinaceous substrates resulting from tissue destruction.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Amino acids are fermented to produce short‐chain fatty acids, such as propionate, butyrate, succinate, acetate, and formate.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Amino acid fermentation neutralizes acidic environments, making the environment more favorable for outgrowth of additional periodontitis‐associated pathogens.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“Deepening of the gingival crevice and increased production of gingival crevicular fluid increases the relative abundance of protein‐degrading bacteria.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [8]
In the citing paper
“For instance, saccharolytic (sugar metabolizing) bacteria such as Streptococcus and Lactobacillus have been associated with dental caries, while proteolytic (protein metabolizing) bacteria such as Prevotella and Porphyromonas have been associated with periodontitis and halitosis[183].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [183]
In the citing paper
“Yet, individual bacteria do not act in a vacuum, but rather function in interdependent microbial communities whose conglomerate activity can impact oral and systemic health[183,188,189].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [183]
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Microbial metabolites in the pathogenesis of periodontal diseases: a narrative review
Basic, A., & Dahlén, G. (2023) · Frontiers in Oral Health · doi:10.3389/froh.2023.1210200 · Cited by 87
Ye, W., Zhang, Y., He, M., Zhu, C., & Feng, X. (2019) · Journal of Breath Research · doi:10.1088/1752-7163/ab47b4 · Cited by 77
The Complicated Relationship of Short-Chain Fatty Acids and Oral Microbiome: A Narrative Review
Leonov, G. E., Varaeva, Y. R., Николаевна, Л. Е., & Starodubova, A. V. (2023) · Biomedicines · doi:10.3390/biomedicines11102749 · Cited by 78
“Carbohydrates undergo fermentation, leading to the formation of monosaccharides, followed by the conversion to pyruvate through either the pentose phosphate pathway (C5) or glycolysis (C6) [44].”
BackgroundIn-vivo shift of the microbiota in oral biofilm in response to frequent sucrose consumption
Anderson, A. C., Rothballer, M., Altenburger, M. J., Woelber, J. P., Karygianni, L., Lagkouvardos, I., Hellwig, E., & Al‐Ahmad, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-32544-6 · Cited by 74
Oral Microbiome Studies: Potential Diagnostic and Therapeutic Implications
Mira, Á. (2018) · Advances in Dental Research · doi:10.1177/0022034517737024 · Cited by 72
Propionate and Alzheimer’s Disease
Killingsworth, J., Sawmiller, D. R., & Shytle, R. D. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.580001 · Cited by 76
“As for the oral microbiome, oral microbiota can produce propionate (Takahashi, 2015).”
BackgroundTagaino, R., Washio, J., Abiko, Y., Tanda, N., Sasaki, K., & Takahashi, N. (2019) · Scientific Reports · doi:10.1038/s41598-019-46790-9 · Cited by 70
Self-citationNitrite-producing oral microbiome in adults and children
Sato-Suzuki, Y., Washio, J., Wicaksono, D. P., Sato, T., Fukumoto, S., & Takahashi, N. (2020) · Scientific Reports · doi:10.1038/s41598-020-73479-1 · Cited by 73
Self-citationNegrini, T. D. C., Carlos, I. Z., Duque, C., Caiaffa, K. S., & Arthur, R. A. (2021) · Frontiers in Oral Health · doi:10.3389/froh.2021.697428 · Cited by 82
Schamarek, I., Anders, L., Chakaroun, R., Kovacs, P. L., & Rohde‐Zimmermann, K. (2023) · Nutrition Journal · doi:10.1186/s12937-023-00856-7 · Cited by 73
Acidogenic Potential of Oral Bifidobacterium and Its High Fluoride Tolerance
Manome, A., Abiko, Y., Kawashima, J., Washio, J., Fukumoto, S., & Takahashi, N. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01099 · Cited by 69
“…bacteria, such as S. mutans, metabolize carbohydrates through glycolysis (the Embden-Meyerhof-Parnas pathway) and mainly produce lactate (Takahashi, 2015), whereas Bifidobacterium species were reported to metabolize carbohydrates through the bifid shunt, which produces both acetate and…”
BackgroundSelf-citationMetabolites of the oral microbiome: important mediators of multikingdom interactions
Barbour, A., Elebyary, O., Fine, N. A., Oveisi, M., & Glogauer, M. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab039 · Cited by 73
The dental calculus metabolome in modern and historic samples
Velsko, I. M., Overmyer, K. A., Speller, C., Klaus, L., Collins, M. J., Loe, L., Frantz, L., Sankaranarayanan, K., Lewis, C. M., Martinez, J. B. R., et al. (2017) · Metabolomics · doi:10.1007/s11306-017-1270-3 · Cited by 68
Kunath, B. J., Hickl, O., Queirós, P., Martin‐Gallausiaux, C., Lebrun, L., Halder, R., Laczny, C. C., Schmidt, T., Hayward, M. R., Becher, D., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01435-4 · Cited by 70
In vitro biofilm models to study dental caries: a systematic review
Maske, T. T., van de Sande, F. H., Arthur, R. A., Huysmans, M. C. D. N. J. M., & Cenci, M. S. (2017) · Biofouling · doi:10.1080/08927014.2017.1354248 · Cited by 73
Dental caries and their microbiomes in children: what do we do now?
Ribeiro, A. A., & Paster, B. J. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2023.2198433 · Cited by 73
Li, W., & Ma, Z. S. (2020) · Scientific Reports · doi:10.1038/s41598-019-56561-1 · Cited by 66
Determining bacterial and host contributions to the human salivary metabolome
Gardner, A., Parkes, H. G., So, P., & Carpenter, G. H. (2019) · Journal of Oral Microbiology · doi:10.1080/20002297.2019.1617014 · Cited by 67
Hu, C., Wang, L., Lin, Y., Liang, H., Zhou, S., Zheng, F., Feng, X., Rui, Y., & Shao, L. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201901301 · Cited by 65
Flossing Is Associated with Improved Oral Health in Older Adults
Marchesan, J. T., Byrd, K. M., MOSS, K. L., Preisser, J. S., Morelli, T., Zandoná, A. F., Jiao, Y., & Beck, J. D. (2020) · Journal of Dental Research · doi:10.1177/0022034520916151 · Cited by 65
“…microbial biofilm are a fundamental etiology (Loe et al. 1965; Beck and Drake 1975; Listgarten et al. 1975; Hunt et al. 1992; Guggenheim et al. 2004; Socransky and Haffajee 2005; Curtis et al. 2011; Hajishengallis et al. 2012; Jiao et al. 2013; Teles et al. 2013; Takahashi 2015; Sanz et al. 2017).”
BackgroundBacteria and Methanogens in the Human Microbiome: a Review of Syntrophic Interactions
Djemai, K., Drancourt, M., & Alou, M. T. (2021) · Microbial Ecology · doi:10.1007/s00248-021-01796-7 · Cited by 64
Chen, L., Xu, X., Wu, X., Cao, H., Li, X., Hou, Z., Wang, B., Liu, J., Ji, X., Zhang, P., et al. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.942460 · Cited by 67
“Lactobacillus is a supragingival saccharolytic bacteria that degrades carbohydrates (such as sugars) into organic acids as well as metabolizing amino acids into acids and ammonia, thus leading to the demineralization of tooth surfaces and the development of caries (Takahashi, 2015).”
BackgroundXu, H., Tian, J., Hao, W., Zhang, Q., Zhou, Q., Shi, W., Qin, M., He, X., & Chen, F. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02009 · Cited by 63
“In all, recent advances in molecular biology have facilitated the profiling of the caries-related oral microbiome (Yang et al., 2012), however, the respect function and roles of these caries-associated species in disease onset and development are still poorly understood (Takahashi, 2015).”
BackgroundBacterial Composition and Metabolomics of Dental Plaque From Adolescents
Havsed, K., Stensson, M., Jansson, H., Carda‐Diéguez, M., Pedersen, A., Neilands, J., Svensäter, G., & Mira, Á. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.716493 · Cited by 63
“Other authors have advised that microbial analysis of oral samples should assess not only the taxonomic composition but also their functional features (Takahashi, 2015; Nascimento et al., 2017).”
BackgroundCurrent State and Challenges of the Global Outcomes of Dental Caries Research in the Meta-Omics Era
Moussa, D. G., Ahmad, P., Mansour, T. A., & Siqueira, W. L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.887907 · Cited by 64
“The Takahashi group presented a number of in-vitro and in-vivo studies aiming to explore a metabolite signature for caries activity in the June 2022 | Volume 12 | Article 887907 supragingival plaque biofilm using an MS-based method (Figure 2) (Takahashi et al., 2012; Takahashi, 2015).”
BackgroundMethodDysbiosis of Oral Microbiota and Metabolite Profiles Associated with Type 2 Diabetes Mellitus
Li, Y., Qian, F., Cheng, X., Wang, D., Wang, Y., Pan, Y., Chen, L., Wang, W., & Tian, Y. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.03796-22 · Cited by 62
Metabolic interplay of SCFA’s in the gut and oral microbiome: a link to health and disease
Nireeksha, Luke, A. M., Kumari, S., Hegde, M. N., & Hegde, N. N. (2025) · Frontiers in Oral Health · doi:10.3389/froh.2025.1646382 · Cited by 76
“Increased SCFA concentrations and the periodontopathogen load in plaque bio fi lms are strongly correlated, suggesting that although SCFAs are advantageous in moderation, excessive synthesis might have negative effects ( 26, 27).”
Bostanghadiri, N., Kouhzad, M., Taki, E., Elahi, Z., Khoshbayan, A., Navidifar, T., & Darban-Sarokhalil, D. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1431785 · Cited by 61
“In addition, it has also been contributed to various types of malignancies, including gastric, colorectal, liver, lung, esophageal, and breast malignancies (Takahashi, 2015).”
BackgroundMethodSecond Era of OMICS in Caries Research: Moving Past the Phase of Disillusionment
Nascimento, M. M., Zaura, E., Mira, Á., Takahashi, N., & ten Cate, J. M. (2017) · Journal of Dental Research · doi:10.1177/0022034517701902 · Cited by 60
“A more comprehensive catalogue of metabolic pathways of oral bacteria was published subsequently (Takahashi 2015).”
BackgroundSelf-citationTian, J., Utter, D. R., Cen, L., Dong, P., Shi, W., Bor, B., Qin, M., McLean, J. S., & He, X. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114909119 · Cited by 62
Costa, R. C., Bertolini, M., Oliveira, B. E. C., NAGAY, B. E., Dini, C., Benso, B., Klein, M. I., Barão, V. A. R., & Souza, J. G. S. (2022) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2022.2062219 · Cited by 62
“The a1-3 glucans have been considered as a “biological glue”, binding the cells through cell-surface proteins that work as glucan-receptors (Takahashi 2015; MatsumotoNakano 2018).”
BackgroundOral microbiome variations related to ageing: possible implications beyond oral health
Kazarina, A., Kuzmicka, J., Bortkevica, S., Zayakin, P., Ķimsis, J., Igumnova, V., Sadovska, D., Freimane, L., Kivrāne, A., Namiņa, A., et al. (2023) · Archives of Microbiology · doi:10.1007/s00203-023-03464-5 · Cited by 59
“Within the oral cavity, Lactobacillus is a common causal agent of dental caries, metabolizing carbohydrates into organic acids (Takahashi 2015).”
BackgroundGualtero, D. F., Lafaurie, G. I., Buitrago, D. M., Castillo, Y., Sanchez, P. K. V., & Castillo, D. M. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1250263 · Cited by 62
“As discussed above, an imbalance in NO bioavailability associated with oral microbiome dysbiosis is associated with some cardiovascular and metabolic diseases (21, 22).”
BackgroundEghbalpoor, F., Gorji, M., Alavigeh, M. Z., & Moghadam, M. T. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e35666 · Cited by 56
“Furthermore, systemic inflammation activates neutrophils, which are part of the innate immune defense and are responsible for identifying and eliminating microorganisms, to release their enzymes, such as neutrophil elastase (NE), myeloperoxidase (MPO), and matrix metalloproteinases (MMPs) [53,54].”
BackgroundHan, Q., Li, B., Zhou, X., Yang, G., Wang, S., Li, M., Ren, B., Wang, H., Zhang, K., Xu, H. H. K., et al. (2017) · Materials · doi:10.3390/ma10060643 · Cited by 56
Shouval, R., Eshel, A., Dubovski, B., Kuperman, A. A., Danylesko, I., Fein, J. A., Fried, S., Geva, M., Kouniavski, E., Neuman, H., et al. (2020) · Blood Advances · doi:10.1182/bloodadvances.2020001827 · Cited by 56
“Microbial metabolites regulate epithelial homeostasis and immune activation and possibly contribute to post-HSCT outcomes.(20-22) Therefore, we sought to study the salivary metabolic profile of patients with and without severe OM (ie, grade 0-1 and 3-4, respectively).”
BackgroundOral microbiome in human health and diseases
Tian, S., Ding, T., & Li, H. (2024) · mLife · doi:10.1002/mlf2.12136 · Cited by 65
Clinical Perspectives of Digital Dermatitis in Dairy and Beef Cattle
Plummer, P. J., & Krull, A. C. (2017) · Veterinary Clinics of North America Food Animal Practice · doi:10.1016/j.cvfa.2017.02.002 · Cited by 55
“Additionally, as these organisms transition the microenvironment to an anaerobic one, they also transition the overall metabolic profiles of the bacterial community from largely saccharolytic (use glucose and sugars for energy) to one that relies more heavily on proteolytic metabolism of proteins.(66) This transition…”
BackgroundGlycaemic status affects the subgingival microbiome of diabetic patients
Longo, P. L., Dabdoub, S. M., Kumar, P., Artese, H. P. C., Dib, S. A., Romito, G. A., & Mayer, M. P. A. (2018) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12908 · Cited by 56
“Nutrition of subgingival microorganisms depends basically on GCF, desquamated epithelial and microbial products, and these are usually not subject to elevated glucose levels, like those in supragingival sites (Takahashi, 2015).”
Background
Metadata
- Authors
- Takahashi, N.
- Affiliations
- Tohoku University (JP)
- Corresponding author
- Takahashi, N.
- ORCID
- Takahashi, N.
- Venue
- Journal of Dental Research
- Publisher
- SAGE Publications
- Published
- 2015-09-16
- Volume
- 94
- Issue
- 12
- Pages
- 1628-1637
- ISSN
- 0022-0345 (ISSN-L)
- 1544-0591
- OpenAlex
- W2177799539
- Semantic Scholar
- 07829a891f6241d91d38c3b9b26b4c8d9c2bf4a9
- Cited by
- 488
- References
- 65
- Citations by year
- 2026: 45 · 2025: 65 · 2024: 49 · 2023: 49 · 2022: 55 · 2021: 50 · 2020: 43 · 2019: 48 · 2018: 27 · 2017: 38 · 2016: 16 · 2015: 2
- FWCI
- 4.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Dental Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (26293439)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › General Dentistry › Dental Health and Care Utilization
- Keywords
- oral microbiota, microbial metabolism, dental caries, periodontitis, halitosis, arginine deiminase system, urease, short-chain fatty acids, acetaldehyde, nitrite, Streptococcus, Lactobacillus, Porphyromonas, Prevotella, glycolysis, microbial metabolomics
- MeSH terms
- Bacteria, Dental Caries, Dental Plaque, Humans, Mouth, Oral Health, Periodontal Diseases, Microbiota
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