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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These bacteria can cause demineralization of dental enamel and development of carious lesions, and 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.
“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]
Proteins are broken down into peptides and amino acids (aspartate, serine, and cysteine) through the action of host proteases and peptidases.
“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]
The degradation of protein substrates plays an important role in the pathogenesis of periodontal disease.
“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]
Fermentation of amino acids neutralizes acidic environments, creating a more favorable atmosphere for the growth of other periodontitis pathogens.
“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]
Amino acids are fermented to generate short-chain fatty acids, such as propionate, butyrate, succinate, acetate, and formate.
“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]
Increased depth of the gingival pocket and increased production of gingival crevicular fluid induces an increase in bacteria involved in protein degradation.
“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]
Over 250 species from the oral cavity have been isolated in culture and characterized, including key pathogens such as Streptococcus mutans, Porphyromonas gingivalis, Tannerella forsythia, and Aggregatibacter actinomycetemcomitans, involved in the etiology of dental caries and periodontal disease.
“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]
Processed carbohydrate consumption has been associated with increased incidence of periodontal disease.
“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]
Digestion of starch is initiated in the oral cavity by salivary alpha-amylase, which catalyzes hydrolysis of starch by cleaving alpha-1,4-glycosidic linkages to yield smaller saccharide moieties such as maltose, maltotriose, and alpha-limit dextrins, which can be utilized by early biofilm colonizers and some periodontal pathogens.
“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]
Such processes encourage outgrowth of acidogenic bacteria, such as S mutans, lactobacilli, and bifidobacteria, that enhance the carcinogenicity of dental plaque.
“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]
Pathways in which sugar is metabolized are also shared among some periodontal pathogens, such as Fusobacterium and Prevotella, which can likewise cause acidification.
“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]
During development of periodontal disease, protein-rich and neutral-alkaline environmental pressures promote outgrowth of periodontal pathogens.
“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]
Inflammatory processes promote outgrowth of inflammophilic bacteria via production of proteinaceous substrates resulting from tissue destruction.
“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]
Amino acids are fermented to produce short-chain fatty acids, such as propionate, butyrate, succinate, acetate, and formate.
“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]
Amino acid fermentation neutralizes acidic environments, making the environment more favorable for outgrowth of additional periodontitis-associated pathogens.
“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]
Deepening of the gingival crevice and increased production of gingival crevicular fluid increases the relative abundance of protein-degrading bacteria.
“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]
Saccharolytic bacteria such as Streptococcus and Lactobacillus have been associated with dental caries, while proteolytic bacteria such as Prevotella and Porphyromonas have been associated with periodontitis and halitosis.
“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]
Individual bacteria function in interdependent microbial communities whose conglomerate activity can impact oral and systemic health.
“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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“[216,217].”
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Role of microbial communities in the pathogenesis of periodontal diseases and caries
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Antimicrobial Tolerance and Metabolic Adaptations in Microbial Biofilms
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The salivary microbiota in health and disease
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Integrated hypothesis of dental caries and periodontal diseases
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“This protein-rich environment enhances the growth of indigenous proteolytic and amino acid-degrading bacteria, such as Fusobacterium and Prevotella, the alkaline cytotoxic products of which raise the average pH to around neutral values.”
BackgroundInfluentialSelf-citationMicrobiomes of Site-Specific Dental Plaques from Children with Different Caries Status
Richards, V. P., Alvarez, A. J., Luce, A. R., Bedenbaugh, M., Mitchell, M. L., Burne, R. A., & Nascimento, M. M. (2017) · Infection and Immunity · doi:10.1128/iai.00106-17 · Cited by 201 · see citing works
A comprehensive review of the application of probiotics and postbiotics in oral health
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“This leads to bacterial aggregation and co-aggregation and the formation of a new biofilm (Twetman, 2012; Piwat et al., 2015; Takahashi, 2015; Morales et al., 2016).”
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Probiotics and oral health: A systematic review
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On the ecosystemic network of saliva in healthy young adults
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Salivary Metabolomics: From Diagnostic Biomarker Discovery to Investigating Biological Function
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“Large increases in free valine are suggestive of proteolysis, and butyrate production may represent the terminal metabolite in a range of amino-acid catabolic pathways, particularly lysine [104,105].”
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“Such bacterial metabolism results in the formation of various compounds, some of which are suggested to participate in the pathogenesis of periodontitis [58].”
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Applications of the oral microbiome in personalized dentistry.
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“770 taxa (Takahashi, 2015)] and the saliva proteome [1000+ proteins (Bostanci & Bao, 2017)], and functional profile of the innate and adaptive immune response.”
BackgroundMolecular Strategies Underlying Porphyromonas gingivalis Virulence
Silva, I. L., & Cascalès, E. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.166836 · Cited by 140 · see citing works
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The oral microbiome: A Lesson in coexistence
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The role of saliva in aroma release and perception
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The use of bacteriophages to biocontrol oral biofilms
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Oral microbial dysbiosis linked to worsened periodontal condition in rheumatoid arthritis patients
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The Microbiome and Blood Pressure: Can Microbes Regulate Our Blood Pressure?
Khodor, S. A., Reichert, B., & Shatat, I. F. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00138 · Cited by 120 · see citing works
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Probiotics: A Promising Role in Dental Health
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From Nitrate to Nitric Oxide: The Role of Salivary Glands and Oral Bacteria
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“However, due to the commensal bacteria that reside within the human body, it has been demonstrated that these bacteria can reduce nitrate, thereby providing an alternative source of nitrite (Goaz and Biswell 1961; Takahashi 2015).”
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The oral cavity microbiota: between health, oral disease, and cancers of the aerodigestive tract
Bars, P. L. L., Matamoros, S., Montassier, E., Vacon, F. L., Potel, G., Soueidan, A., Jordana, F., & de la Cochetière, M.-F. (2017) · Canadian Journal of Microbiology · doi:10.1139/cjm-2016-0603 · Cited by 108 · see citing works
Profiling the Salivary microbiome of the Qatari population
Murugesan, S., Ahmad, S. F. A., Singh, P., Saadaoui, M., Kumar, M., & Khodor, S. A. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-020-02291-2 · Cited by 105 · see citing works
The Saliva Metabolome in Association to Oral Health Status
Liebsch, C., Pitchika, V., Pink, C., Samietz, S., Kastenmüller, G., Artati, A., Suhre, K., Adamski, J., Nauck, M. A., Völzke, H., et al. (2019) · Journal of Dental Research · doi:10.1177/0022034519842853 · Cited by 102 · see citing works
Sugars and beyond. The role of sugars and the other nutrients and their potential impact on caries
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Association between the gut and oral microbiome with obesity
Benahmed, A. G., Gasmi, A., Doşa, A., Chirumbolo, S., Mujawdiya, P. K., Aaseth, J., Dadar, M., & Bjørklund, G. (2020) · Anaerobe · doi:10.1016/j.anaerobe.2020.102248 · Cited by 102 · see citing works
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Carbon Nanotube Based Gas Sensors toward Breath Analysis
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New insights into the relationship between taste perception and oral microbiota composition
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The tongue microbiome in healthy subjects and patients with intra-oral halitosis
Seerangaiyan, K., Winkelhoff, A. J. V., Harmsen, H. J. M., Rossen, J. W. A., & Winkel, E. G. (2017) · Journal of Breath Research · doi:10.1088/1752-7163/aa7c24 · Cited by 91 · see citing works
“Moreover, survival of the species in a particular ecosystem mainly depends on the metabolic activities of the bacteria which results in the formation of a metabolic network based on symbiotic relationship of the species [36].”
BackgroundOral Microbiome in Relation to Periodontitis Severity and Systemic Inflammation
Plachokova, A., Andreu-Sánchez, S., Noz, M. P., Fu, J.-Y., & Riksen, N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115876 · Cited by 83 · see citing works
Oral microbiome, periodontitis and risk of head and neck cancer
Galvão-Moreira, L. V., & da Cruz, M. C. F. N. (2015) · Oral Oncology · doi:10.1016/j.oraloncology.2015.11.013 · Cited by 91 · see citing works
“Still, germ-free rats presented with lower acetaldehyde concentration, indicating that might exist an epidemiologic link between poor oral hygiene, alcohol consumption and increased risk of OCC [2,6].”
BackgroundShort-chain fatty acids and FFAR2 as suppressors of bone resorption
Montalvany-Antonucci, C. C., Duffles, L. F., de Arruda, J. A. A., Zicker, M. C., de Oliveira, S., Macari, S., Garlet, G. P., Madeira, M. F. M., Fukada, S. Y., Andrade, I., et al. (2019) · Bone · doi:10.1016/j.bone.2019.05.016 · Cited by 89 · see citing works
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“Another plausible explanation may lie in bacterial ability to degrade carbohydrates into disaccharides, monosaccharides, and organic acids, used as “building material” for biofilms [61].”
BackgroundNitrite Production from Nitrate and Its Link with Lactate Metabolism in Oral Veillonella spp
Wicaksono, D. P., Washio, J., Abiko, Y., Domon, H., & Takahashi, N. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.01255-20 · Cited by 85 · see citing works
Self-citationThe oral microbiota and cardiometabolic health: A comprehensive review and emerging insights
Li, Y. H., Zhu, M., Liu, Y., Luo, B., Cui, J., Huang, L., Chen, K., & Liu, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1010368 · Cited by 88 · see citing works
Interdental Cleaning Is Associated with Decreased Oral Disease Prevalence
Marchesan, J. T., Morelli, T., MOSS, K. L., Preisser, J. S., Zandoná, A. G. F., Offenbacher, S., & Beck, J. D. (2018) · Journal of Dental Research · doi:10.1177/0022034518759915 · Cited by 83 · see citing works
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Gender-Specific Associations Between Saliva Microbiota and Body Size
Raju, S. C., Lagström, S., Ellonen, P., de Vos, W., Eriksson, J., Weiderpass, E., & Rounge, T. B. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00767 · Cited by 68 · see citing works
“Saccharolytic bacteria–Streptococcus, Actinomyces, and Lactobacillus species—degrade carbohydrates into organic acids, resulting in dental caries (Takahashi, 2015).”
BackgroundOral Microorganisms and Biofilms: New Insights to Defeat the Main Etiologic Factor of Oral Diseases
Bertolini, M., Costa, R. L. G. F. D. C., Barão, V. A. R., Villar, C. C., Retamal‐Valdes, B., Feres, M., & Souza, J. G. S. (2022) · Microorganisms · doi:10.3390/microorganisms10122413 · Cited by 91 · see citing works
“This microorganism can grow in acidic environments with low pH (aciduric) and has a high capacity for acid production (acidogenic), important factors for caries lesion progression [31].”
BackgroundMetabolic traits of pathogenic streptococci
Willenborg, J., & Goethe, R. (2016) · FEBS Letters · doi:10.1002/1873-3468.12317 · Cited by 80 · see citing works
Ecological Therapeutic Opportunities for Oral Diseases
Hoare, A., Marsh, P. D., & Diaz, P. I. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.bad-0006-2016 · Cited by 81 · see citing works
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 84 · see citing works
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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 74 · see citing works
“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 · see citing works
Oral Microbiome Studies: Potential Diagnostic and Therapeutic Implications
Mira, Á. (2018) · Advances in Dental Research · doi:10.1177/0022034517737024 · Cited by 72 · see citing works
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 71 · see citing works
“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 · see citing works
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 70 · see citing works
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 76 · see citing works
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 · see citing works
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 · see citing works
“…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 68 · see citing works
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 · see citing works
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 69 · see citing works
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 67 · see citing works
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 · see citing works
Li, W., & Ma, Z. S. (2020) · Scientific Reports · doi:10.1038/s41598-019-56561-1 · Cited by 65 · see citing works
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 65 · see citing works
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 · see citing works
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 · see citing works
“…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).”
BackgroundBostanghadiri, 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 · see citing works
“In addition, it has also been contributed to various types of malignancies, including gastric, colorectal, liver, lung, esophageal, and breast malignancies (Takahashi, 2015).”
BackgroundMethodBacteria 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 63 · see citing works
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 66 · see citing works
“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 · see citing works
“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 · see citing works
“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 62 · see citing works
“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 · see citing works
Metabolic interplay of SCFA’s in the gut and oral microbiome: a link to health and disease
Nireeksha, Luke, A. M., N, S. K., Hegde, M. N., & Hegde, N. N. (2025) · Frontiers in Oral Health · doi:10.3389/froh.2025.1646382 · Cited by 67 · see citing works
“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).”
Second 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 · see citing works
“A more comprehensive catalogue of metabolic pathways of oral bacteria was published subsequently (Takahashi 2015).”
BackgroundSelf-citationTian, J., Utter, D., Cen, L., Dong, P.-T., Shi, W.-Y., Bor, B., Qin, M., McLean, J., & He, X. (2022) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2114909119 · Cited by 58 · see citing works
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 60 · see citing works
“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 56 · see citing works
“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 56 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
“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 61 · see citing works
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 · see citing works
“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 · see citing works
“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
- 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 › Periodontics › 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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