Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans

Moye, Zachary D.; Zeng, Lin; Burne, Robert A.

doi:10.3402/jom.v6.24878

Cited by 165Oral microbiology and periodontitis researchBacterial Genetics and BiotechnologyDental Health and Care Utilization

Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans

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Moye, Zachary D., Zeng, Lin, Burne, Robert A.·2014·Journal of Oral Microbiology

DOI 10.3402/jom.v6.24878PMC PMC4157138

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Abstract

The nature of the oral cavity and host behaviors has mandated that the oral microbiota evolve mechanisms for coping with environmental fluctuations, especially changes in the type and availability of carbohydrates. In the case of human dental caries, the presence of excess carbohydrates is often responsible for altering the local environment to be more favorable for species associated with the initiation and progression of disease, including Streptococcus mutans. Some of the earliest endeavors to understand how cariogenic species respond to environmental perturbations were carried out using chemostat cultivation, which provides fine control over culture conditions and bacterial behaviors. The development of genome-scale methodologies has allowed for the combination of sophisticated cultivation technologies with genome-level analysis to more thoroughly probe how bacterial pathogens respond to environmental stimuli. Recent investigations in S. mutans and other closely related streptococci have begun to reveal that carbohydrate metabolism can drastically impact pathogenic potential and highlight the important influence that nutrient acquisition has on the success of pathogens; inside and outside of the oral cavity. Collectively, research into pathogenic streptococci, which have evolved in close association with the human host, has begun to unveil the essential nature of careful orchestration of carbohydrate acquisition and catabolism to allow the organisms to persist and, when conditions allow, initiate or worsen disease.

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Saccharolytic bacteria include Streptococcus, Actinomyces, and Veillonella, which have the unique ability to degrade carbohydrates via the Embden-Meyerhof-Pernas pathway, producing acidic by-products including lactate, acetate, ethanol, and formate.
“The saccharolytic bacteria include Streptococcus, Actinomyces, and Veillonella, which have the unique ability to degrade carbohydrates via the Embden−Meyerhof−Pernas pathway, producing acidic by-products including lactate, acetate, ethanol, and formate [1,82].”
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 [1]
Recent data indicate that the oral microbiome influences the dietary preferences of its host.
“While diet influences the oral microbiome,22, 24, 26 recent data indicate that the oral microbiome influences the dietary preferences of its host.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [22]
Diet provides nutritional resources for the oral microbiota and serves as a selective pressure by enriching for organisms best adapted to utilize specific host-derived dietary resources.
“Diet provides nutritional resources for the oral microbiota and also serves as a selective pressure by enriching for organisms best adapted to utilize specific host‐derived dietary resources.22”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [22]
Changes in diet were paralleled by pathologic changes to the oral microbiota, including greater representation of acid-producing and acid-tolerant organisms and periodontal pathogens.
“Such changes in diet were paralleled by pathologic changes to the oral microbiota, including greater representation of acid‐producing and acid‐tolerant organisms and periodontal pathogens.17, 22, 24, 25”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [22]
Carbohydrate use by S mutans is a well-recognized feature in the pathogenicity of dental caries.
“Carbohydrate use by S mutans is a well‐recognized feature in the pathogenicity of dental caries.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [22]

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Abranches, J., Chen, Y. M., & Burne, R. A. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.8.4760-4769.2003 · Cited by 92 · see citing works
A novel adaptation of aldolase regulates virulence in Streptococcus pyogenes
Loughman, J. A., & Caparon, M. G. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601393 · Cited by 90 · cited 2× · see citing works
“1 is primarily believed to serve as a metabolite-sensing co-regulator of enzymes including the DNA-binding regulator Rgg (also called RopB) (124, 125).”
Background
A synthetic saliva for cultural studies of dental plaque
Shellis, R. P. (1978) · Archives of Oral Biology · doi:10.1016/0003-9969(78)90081-x · Cited by 88 · cited 1× · see citing works
“In some instances, these challenges have been overcome by the creation of artificial saliva, and though not as complex as saliva obtained from human subjects, the results obtained with this medium are in some cases comparable to those of human saliva (74, 75).”
Result
Analysis of the nag regulon from Escberichia coli K12 and Klebsiella pneumoniae and of its regulation
Vogler, A. P., & Lengeler, J. W. (1989) · Molecular and General Genetics MGG · doi:10.1007/bf00261163 · Cited by 86 · see citing works
Nucleotide and deduced amino acid sequences of the lacR, lacABCD, and lacFE genes encoding the repressor, tagatose 6-phosphate gene cluster, and sugar-specific phosphotransferase system components of the lactose operon of Streptococcus mutans
Rosey, E. L., & Stewart, G. C. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.19.6159-6170.1992 · Cited by 85 · see citing works
Effect of Growth Rate and Glucose Concentration on the Activity of the Phosphoenolpyruvate Phosphotransferase System in Streptococcus mutans Ingbritt Grown in Continuous Culture
Ellwood, D. C., Phipps, P. J., & Hamilton, I. R. (1979) · Infection and Immunity · doi:10.1128/iai.23.2.224-231.1979 · Cited by 85 · see citing works
The Catabolite Control Protein CcpA Binds to P mga and Influences Expression of the Virulence Regulator Mga in the Group A Streptococcus
Almengor, A. C., Kinkel, T. L., Day, S. J., & McIver, K. S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01038-07 · Cited by 85 · cited 1× · see citing works
“pyogenes possesses a CcpAbinding site upstream of the promoter for mga (130, 131).”
Background
Two Closely Related ABC Transporters in Streptococcus mutans Are Involved in Disaccharide and/or Oligosaccharide Uptake
Webb, A., Homer, K. A., & Hosie, A. H. F. (2007) · Journal of Bacteriology · doi:10.1128/jb.01509-07 · Cited by 84 · see citing works
Streptococcus mutans fructosyltransferase (ftf) and glucosyltransferase (gtfBC) operon fusion strains in continuous culture
Wexler, D. L., Hudson, M. C., & Burne, R. A. (1993) · Infection and Immunity · doi:10.1128/iai.61.4.1259-1267.1993 · Cited by 82 · see citing works
CcpA-Mediated Repression of Streptolysin S Expression and Virulence in the Group A Streptococcus
Kinkel, T. L., & McIver, K. S. (2008) · Infection and Immunity · doi:10.1128/iai.00343-08 · Cited by 81 · cited 1× · see citing works
“Other researchers have observed an enhancement of virulence in the ccpA deletion strain similarly to that exhibited by the ptsI mutant though less severe (123).”
Background
A novel signal transduction system and feedback loop regulate fructan hydrolase gene expression in Streptococcus mutans
Zeng, L., Wen, Z. T., & Burne, R. A. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05359.x · Cited by 79 · cited 1× · see citing works
“The LevQRST fourcomponent system activates fruA and levDEFG expression in response to extracellular signals, including the presence of fructose and mannose, and is sensitive to CcpAindependent catabolite repression (31, 92).”
Background
Rodent model in caries research
Bowen, W. H. (2012) · Odontology · doi:10.1007/s10266-012-0091-0 · Cited by 78 · cited 3× · see citing works
“In addition, studies using rats have illustrated that it is not as much the consumption of particular sugars but the frequency of consumption that strongly contributes to caries, and further, many anti-caries treatments succeed mostly due to their impact on the frequency of meals (78).”
BackgroundInfluential
Pneumococcal carbohydrate transport: food for thought
Buckwalter, C. M., & King, S. J. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.08.008 · Cited by 76 · cited 1× · see citing works
“pneumoniae moves away from the oral cavity and ventures into the airways, it is likely that this pathogen must liberate and metabolize nutrients from host glycoconjugates, including host defense molecules (132).”
Background
Characterization of the Streptococcus mutans GS-5 fruA gene encoding exo-beta-D-fructosidase
Burne, R. A., & Penders, J. E. C. (1992) · Infection and Immunity · doi:10.1128/iai.60.11.4621-4632.1992 · Cited by 75 · cited 1× · see citing works
“mutans produces a secreted exob-D-fructosidase, FruA, that releases fructose from b2, 6 and b2,1-linked fructan polymers (88, 89).”
Background
Uptake and Metabolism of N -Acetylglucosamine and Glucosamine by Streptococcus mutans
Moye, Z. D., Burne, R. A., & Zeng, L. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00820-14 · Cited by 74 · cited 17× · see citing works
“Researchers in the field of oral biology have long known that S. mutans is capable of utilizing both GlcN and GlcNAc, and GlcNAc has classically been utilized as a method for distinguishing S. mutans from the related cariogenic species Streptococcus sobrinus (94, 95).”
BackgroundInfluential
CcpA and LacD.1 Affect Temporal Regulation ofStreptococcus pyogenesVirulence Genes
Kietzman, C. C., & Caparon, M. G. (2009) · Infection and Immunity · doi:10.1128/iai.00746-09 · Cited by 73 · cited 1× · see citing works
“Firstly, CcpA plays an important role in coordinating virulence gene expression, and deletion of ccpA has in some cases been linked to a loss of virulence in murine models of infection (121, 122).”
Background
PTS phosphorylation of Mga modulates regulon expression and virulence in the group A streptococcus
Hondorp, E. R., Hou, S. C., Hause, L. L., Gera, K., Lee, C., & McIver, K. S. (2013) · Molecular Microbiology · doi:10.1111/mmi.12250 · Cited by 72 · cited 2× · see citing works
“pyogenes possesses a CcpAbinding site upstream of the promoter for mga (130, 131).”
Background
Transcriptional Regulation of the Cellobiose Operon of Streptococcus mutans
Zeng, L., & Burne, R. A. (2009) · Journal of Bacteriology · doi:10.1128/jb.01641-08 · Cited by 72 · cited 5× · see citing works
“Likewise, deletion of EIIB was thought to cause constitutive phosphorylation of EIIA, leading to inactivation of CelR (24).”
BackgroundInfluential
Transport of Sugars, Including Sucrose, by the msm Transport System of Streptococcus mutans
Tao, L., Sutcliffe, I. C., Russell, R. R. B., & Ferretti, J. J. (1993) · Journal of Dental Research · doi:10.1177/00220345930720100701 · Cited by 69 · cited 1× · see citing works
“It was demonstrated that the primary PTS permease (EII) for trehalose (a-D-glucopyranosyl1,1-a-D-glucopyranoside) and the msm ABC transporter contributed modestly to growth on sucrose, so these systems appear to function in lower-affinity sucrose uptake, as suggested previously (14, 91).”
Background
Differential response of Streptococcus mutans towards friend and foe in mixed-species cultures
Liu, J., Wu, C., Huang, I., Merritt, J. L., & Qi, F. (2011) · Microbiology · doi:10.1099/mic.0.048314-0 · Cited by 69 · cited 1× · see citing works
“mutans due to the presence of a highaffinity galactose PTS, a trait that may help to promote dental health (108, 109).”
Background
Gene Regulation by CcpA and Catabolite Repression Explored by RNA-Seq in Streptococcus mutans
Zeng, L., Choi, S. C., Danko, C. G., Siepel, A. C., Stanhope, M. J., & Burne, R. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060465 · Cited by 69 · cited 1× · see citing works
“Also of note, a ccpA mutant did not display a similar upregulation of the cel operon when assayed by microarray (29), though a subsequent RNA-Seq study did show modest elevation in cel operon expression upon deletion of ccpA (117).”
Result
Environmental Influences on Competitive Hydrogen Peroxide Production in Streptococcus gordonii
Zheng, L., Itzek, A., Chen, Z., & Kreth, J. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.00309-11 · Cited by 68 · cited 1× · see citing works
“Further, carbohydrate sources have been demonstrated to impact the ability of the pathogen to antagonize commensals via the production of bacteriocins (139) and conversely, the capacity of commensals to respond through the production of defensive compounds, such as hydrogen peroxide (140, 141).”
Background
Seryl‐phosphorylated HPr regulates CcpA‐independent carbon catabolite repression in conjunction with PTS permeases in Streptococcus mutans
Zeng, L., & Burne, R. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.07029.x · Cited by 67 · cited 1× · see citing works
“mutans, serinephosphorylated HPr (HPr(Ser-P)) plays a major role in the repression of genes for the uptake and metabolism of non-preferred carbohydrate sources (28).”
Background
Utilization of mucin by oral Streptococcus species
van der Hoeven, J. S., van den Kieboom, C. W. A., & Camp, P. J. M. (1990) · Antonie van Leeuwenhoek · doi:10.1007/bf00403951 · Cited by 63 · cited 3× · see citing works
“mutans may exploit mucin as a supplementary nutrient source during fasting periods by the host, though not as the sole carbon and energy source (71).”
Background
Effect of growth conditions on the formation of extracellular lipoteichoic acid by Streptococcus mutans BHT
Jacques, N. A., HARDY, L. N., Knox, K. W., & Wicken, A. J. (1979) · Infection and Immunity · doi:10.1128/iai.25.1.75-84.1979 · Cited by 63 · see citing works
Regulon of the N -Acetylglucosamine Utilization Regulator NagR in Bacillus subtilis
Bertram, R., Rigali, S., Wood, N., Lulko, A. T., Kuipers, O. P., & Titgemeyer, F. (2011) · Journal of Bacteriology · doi:10.1128/jb.00264-11 · Cited by 62 · see citing works
Comprehensive Mutational Analysis of Sucrose-Metabolizing Pathways in Streptococcus mutans Reveals Novel Roles for the Sucrose Phosphotransferase System Permease
Zeng, L., & Burne, R. A. (2012) · Journal of Bacteriology · doi:10.1128/jb.02042-12 · Cited by 61 · cited 4× · see citing works
“mutans, particularly when cells are grown in the presence of the sugar(s) that are internalized by these permeases (21, 30, 31).”
BackgroundInfluential
Glucose transport by a mutant of Streptococcus mutans unable to accumulate sugars via the phosphoenolpyruvate phosphotransferase system
Cvitkovitch, D. G., Boyd, D. A., Thevenot, T., & Hamilton, I. R. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.9.2251-2258.1995 · Cited by 59 · cited 1× · see citing works
“which is active in PTS-deficient cells (66), it is likely that”
Background
Mutation of the NADH Oxidase Gene ( nox ) Reveals an Overlap of the Oxygen- and Acid-Mediated Stress Responses in Streptococcus mutans
Derr, A. M., Faustoferri, R. C., Betzenhauser, M. J., Gonzalez, K., Marquis, R. E., & Quivey, R. G. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.06890-11 · Cited by 58 · cited 1× · see citing works
“mutans in response to selected growth conditions, including an acidic environment (61, 62), of the GlnR-mediated response to low pH (63) and of the contribution of NADH oxidase to acid and oxidative stress (64).”
Background
The Two-Component Regulatory System TCS08 Is Involved in Cellobiose Metabolism ofStreptococcus pneumoniaeR6
McKessar, S. J., & Hakenbeck, R. (2007) · Journal of Bacteriology · doi:10.1128/jb.01170-06 · Cited by 58 · cited 1× · see citing works
“mutans and Streptococcus pneumoniae is necessary for the efficient internalization of cellobiose (23, 24).”
Background
An expanded collection and refined consensus model of glmS ribozymes
McCown, P. J., Roth, A., & Breaker, R. R. (2011) · RNA · doi:10.1261/rna.2590811 · Cited by 58 · cited 2× · see citing works
“coli and other members of Enterobacteriaceae (103, 104), or by a metabolitebinding ribozyme in many Gram-positive organisms (105, 106).”
Background
Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae
Göpel, Y., Lüttmann, D., Heroven, A. K., Reichenbach, B., Dersch, P., & Görke, B. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq986 · Cited by 58 · cited 2× · see citing works
“coli and other members of Enterobacteriaceae (103, 104), or by a metabolitebinding ribozyme in many Gram-positive organisms (105, 106).”
Background
Effect of Growth Rate and Glucose Concentration on the Biochemical Properties of Streptococcus mutans Ingbritt in Continuous Culture
Hamilton, I. R., Phipps, P. J., & Ellwood, D. C. (1979) · Infection and Immunity · doi:10.1128/iai.26.3.861-869.1979 · Cited by 57 · cited 1× · see citing works
“stores (65), closely resembling previous results (46).”
Effect of fructose and other carbohydrates on the surface properties, lipoteichoic acid production, and extracellular proteins of Streptococcus mutans Ingbritt grown in continuous culture
HARDY, L. N., Jacques, N. A., Forester, H., Campbell, L. K., Knox, K. W., & Wicken, A. J. (1981) · Infection and Immunity · doi:10.1128/iai.31.1.78-87.1981 · Cited by 56 · see citing works
Multiple Phosphorylation Events Regulate the Activity of the Mannitol Transcriptional Regulator MtlR of the Bacillus stearothermophilus Phosphoenolpyruvate-dependent Mannitol Phosphotransferase System
Henstra, S. A., Duurkens, R. H., & Robillard, G. T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.10.7037 · Cited by 55 · see citing works
Oxygen toxicity in Streptococcus mutans: manganese, iron, and superoxide dismutase
Martin, M. E., Strachan, R. C., Aranha, H., Evans, S. L., Salin, M. L., Welch, B. G., Arceneaux, J. E. L., & Byers, B. R. (1984) · Journal of Bacteriology · doi:10.1128/jb.159.2.745-749.1984 · Cited by 54 · see citing works
Sucrose metabolism by Streptococcus mutans, SL-I
Tanzer, J. M., Chassy, B. M., & Krichevsky, M. I. (1972) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(72)90062-1 · Cited by 53 · cited 1× · see citing works
“mutans is internalized and metabolized to produce organic acids, with a relatively minor portion being converted to extracellular polymers (90), at least in in vitro studies.”
Background
Quantitative determination of the intracellular concentration of the various forms of HPr, a phosphocarrier protein of the phosphoenolpyruvate: Sugar phosphotransferase system in growing cells of oral streptococci
Vadeboncoeur, C., Brochu, D., & Reizer, J. (1991) · Analytical Biochemistry · doi:10.1016/0003-2697(91)90112-7 · Cited by 53 · cited 1× · see citing works
“been noted with batch-grown cells (68).”
Response of Freshly Isolated Strains of Streptococcus mutans and Streptococcus mitior to Change in pH in the Presence and Absence of Fluoride During Growth in Continuous Culture
Hamilton, I. R., & Bowden, G. H. W. (1982) · Infection and Immunity · doi:10.1128/iai.36.1.255-262.1982 · Cited by 53 · see citing works
Comparative functional analysis of the lac operons in Streptococcus pyogenes
Loughman, J. A., & Caparon, M. G. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05663.x · Cited by 52 · cited 2× · see citing works
“1 is primarily believed to serve as a metabolite-sensing co-regulator of enzymes including the DNA-binding regulator Rgg (also called RopB) (124, 125).”
Background
The Bacillus stearothermophilus Mannitol Regulator, MtlR, of the Phosphotransferase System
Henstra, S. A., Tuinhof, M., Duurkens, R. H., & Robillard, G. T. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.8.4754 · Cited by 51 · see citing works
Multiple sugar: phosphotransferase system permeases participate in catabolite modification of gene expression in Streptococcus mutans
Zeng, L., & Burne, R. A. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06403.x · Cited by 51 · cited 3× · see citing works
“In particular, CcpA has the ability to indirectly influence non-preferred sugar uptake by regulating the expression of multiple EII permeases (31).”
Background
Cellular and extracellular proteome analysis of Streptococcus mutans grown in a chemostat
Len, A. C. L., Cordwell, S. J., Harty, D. W. S., & Jacques, N. A. (2003) · PROTEOMICS · doi:10.1002/pmic.200300391 · Cited by 50 · cited 1× · see citing works
“mutans in response to selected growth conditions, including an acidic environment (61, 62), of the GlnR-mediated response to low pH (63) and of the contribution of NADH oxidase to acid and oxidative stress (64).”
Background
Modification of Gene Expression and Virulence Traits in Streptococcus mutans in Response to Carbohydrate Availability
Moye, Z. D., Zeng, L., & Burne, R. A. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03579-13 · Cited by 50 · cited 6× · see citing works
“and excess carbohydrate conditions (65), and these”
BackgroundMethodInfluential
Effect of trace metals on growth of Streptococcus mutans in a teflon chemostat
Aranha, H., Strachan, R. C., Arceneaux, J. E. L., & Byers, B. R. (1982) · Infection and Immunity · doi:10.1128/iai.35.2.456-460.1982 · Cited by 46 · see citing works
Effects of N-acetylglucosamine on carbohydrate fermentation by Streptococcus mutans NCTC 10449 and Streptococcus sobrinus SL-1
Homer, K. A., Patel, R., & Beighton, D. (1993) · Infection and Immunity · doi:10.1128/iai.61.1.295-302.1993 · Cited by 46 · see citing works
GlmS and NagB Regulate Amino Sugar Metabolism in Opposing Directions and Affect Streptococcus mutans Virulence
Kawada‐Matsuo, M., Mazda, Y., Oogai, Y., Kajiya, M., Kawai, T., Yamada, S., Miyawaki, S., Oho, T., & Komatsuzawa, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033382 · Cited by 45 · cited 3× · see citing works
“Analysis of the genomes of multiple Grampositive species has revealed that the canonical residues for the formation of the ribozyme structure are notably absent in species of streptococci and most species in the genus Lactobacillus (98, 105).”
Background
Effect of carbohydrate source and growth conditions on the production of lipoteichoic acid by Streptococcus mutans Ingbritt
Jacques, N. A., HARDY, L. N., Campbell, L. K., Knox, K. W., Evans, J. D., & Wicken, A. J. (1979) · Infection and Immunity · doi:10.1128/iai.26.3.1079-1087.1979 · Cited by 44 · see citing works
Regulation of ATP-dependent P-(Ser)-HPr formation in Streptococcus mutans and Streptococcus salivarius
Thevenot, T., Brochu, D., Vadeboncoeur, C., & Hamilton, I. R. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.10.2751-2759.1995 · Cited by 44 · see citing works
Persistence of Streptococcus mutans in Stationary-Phase Batch Cultures and Biofilms
Renye, J. A., Piggot, P. J., Daneo-moore, L., & Buttaro, B. A. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.10.6181-6187.2004 · Cited by 38 · cited 1× · see citing works
“mutans cannot grow well with mucin as a sole carbon and energy source (71), when mucin was added to sucrose-starved biofilms, the bacteria displayed enhanced survival (72).”
Background
Regulation of Glucosyl- and Fructosyltransferase Synthesis by Continuous Cultures of Streptococcus mutans
WENHAM, D. G., Hennessey, T. D., & Cole, J. A. (1979) · Journal of General Microbiology · doi:10.1099/00221287-114-1-117 · Cited by 37 · see citing works
Cloning, expression, and isolation of the mannitol transport protein from the thermophilic bacterium Bacillus stearothermophilus
Henstra, S. A., Tolner, B., Duurkens, R. H., Konings, W. N., & Robillard, G. T. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.19.5586-5591.1996 · Cited by 36 · see citing works
Two Gene Clusters Coordinate Galactose and Lactose Metabolism in Streptococcus gordonii
Zeng, L., Martino, N., & Burne, R. A. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.01393-12 · Cited by 36 · cited 1× · see citing works
“mutans due to the presence of a highaffinity galactose PTS, a trait that may help to promote dental health (108, 109).”
Background
Effect of growth conditions on levels of components of the phosphoenolpyruvate:sugar phosphotransferase system in Streptococcus mutans and Streptococcus sobrinus grown in continuous culture
Vadeboncoeur, C., Thibault, L., Néron, S., Halvorson, H. O., & Hamilton, I. R. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.12.5686-5691.1987 · Cited by 34 · see citing works
Role of GlnR in Acid-Mediated Repression of Genes Encoding Proteins Involved in Glutamine and Glutamate Metabolism inStreptococcus mutans
Chen, P., Chen, Y. M., Yu, S., Singh, S., Lai, C.-H., & Chia, J. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.02622-09 · Cited by 34 · cited 1× · see citing works
“mutans in response to selected growth conditions, including an acidic environment (61, 62), of the GlnR-mediated response to low pH (63) and of the contribution of NADH oxidase to acid and oxidative stress (64).”
Background
Sucrose, the arch criminal of dental caries.
Newbrun, E. (1969) · PubMed · Cited by 33 · see citing works
Improved Artificial Saliva for Studying the Cariogenic Effect of Carbohydrates
Björklund, M., Ouwehand, A. C., & Forssten, S. D. (2011) · Current Microbiology · doi:10.1007/s00284-011-9937-x · Cited by 31 · cited 2× · see citing works
“mutans cannot survive with mucin as a sole source of carbohydrates (71) and fares much better in artificial and human saliva supplemented with carbohydrates (75).”
BackgroundResult
Properties of Streptococcus mutans Ingbritt growing on limiting sucrose in a chemostat: repression of the phosphoenolpyruvate phosphotransferase transport system
Ellwood, D. C., & Hamilton, I. R. (1982) · Infection and Immunity · doi:10.1128/iai.36.2.576-581.1982 · Cited by 30 · see citing works
Streptococcus mutans serotype c tagatose 6-phosphate pathway gene cluster
Jagusztyn-Krynicka, E. K., Hansen, J. B., Crow, V. L., Thomas, T. D., Honeyman, A. L., & Curtiss, R. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.19.6152-6158.1992 · Cited by 29 · see citing works
Membrane sequestration by the EIIB domain of the mannitol permease MtlA activates the B acillus subtilis mtl operon regulator MtlR
Bouraoui, H., Ventroux, M., Noirot‐Gros, M., Deutscher, J., & Joyet, P. (2012) · Molecular Microbiology · doi:10.1111/mmi.12131 · Cited by 29 · cited 1× · see citing works
“In a recent study of the homologous PRDcontaining regulator MtlR of Bacillus subtilis (118), it was reported that membrane sequestration of MtlR by a dephosphorylated EIIB is essential for full functionality of MtlR and the subsequent activation of downstream catabolic genes.”
Background
Distinct Time-Resolved Roles for Two Catabolite-Sensing Pathways during Streptococcus pyogenes Infection
Kietzman, C. C., & Caparon, M. G. (2010) · Infection and Immunity · doi:10.1128/iai.01026-10 · Cited by 29 · cited 1× · see citing works
“These differences were perhaps mediated by the regulators sensing and responding to different environmental signals, such as glucose, during the course of infection, and may also be influenced by the site of infection (129).”
Background
Evidence that a low-affinity sucrose phosphotransferase activity in Streptococcus mutans GS-5 is a high-affinity trehalose uptake system
Poy, F., & Jacobson, G. R. (1990) · Infection and Immunity · doi:10.1128/iai.58.5.1479-1480.1990 · Cited by 28 · cited 1× · see citing works
“It was demonstrated that the primary PTS permease (EII) for trehalose (a-D-glucopyranosyl1,1-a-D-glucopyranoside) and the msm ABC transporter contributed modestly to growth on sucrose, so these systems appear to function in lower-affinity sucrose uptake, as suggested previously (14, 91).”
Background
The Phosphoenolpyruvate Phosphotransferase System in Group A Streptococcus Acts To Reduce Streptolysin S Activity and Lesion Severity during Soft Tissue Infection
Gera, K., Le, T., Jamin, R., Eichenbaum, Z., & McIver, K. S. (2013) · Infection and Immunity · doi:10.1128/iai.01271-13 · Cited by 28 · cited 1× · see citing works
“pyogenes has implicated EI (ptsI) in the regulation of the sag operon, which produces the streptolysin S (SLS) toxin (119), while HPr is considered absolutely required for growth; as has been demonstrated in S.”
Method
Biochemical Differentiation of Certain Oral Streptococci
Kral, T. A., & Daneo-Moore, L. (1981) · Journal of Dental Research · doi:10.1177/00220345810600091301 · Cited by 26 · cited 1× · see citing works
“mutans from the related cariogenic species Streptococcus sobrinus (94, 95).”
Background
A novel phosphotransferase system of S treptococcus mutans is responsible for transport of carbohydrates with α‐1,3 linkage
Ajdić, D., & Chen, Z. (2012) · Molecular Oral Microbiology · doi:10.1111/omi.12009 · Cited by 26 · cited 4× · see citing works
“Thus, PTSBio appears to transport oligosaccharides that could arise from the action of the GTFs (93), while other genes in the cluster are required for catabolism of the sugars.”
BackgroundInfluential
Effect of nutritional constraints on the biosynthesis of the components of the phosphoenolpyruvate: sugar phosphotransferase system in a fresh isolate of Streptococcus mutans
Rodrigue, L., Lacoste, L., Trahan, L., & Vadeboncoeur, C. (1988) · Infection and Immunity · doi:10.1128/iai.56.2.518-522.1988 · Cited by 25 · see citing works
Mucin can enhance growth, biofilm formation, and survival ofStreptococcus mutans
Mothey, D., Buttaro, B. A., & Piggot, P. J. (2013) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12336 · Cited by 25 · cited 1× · see citing works
“mutans, and this benefit required the presence of an intact tagatose pathway (110), which is a primary route for galactose catabolism in S.”
Background
Activity of Streptococcus mutans a-D-Glucosyltransferases Released Under Various Growth Conditions
Walker, G. J., BROWN, R. A., & Taylor, C. A. (1984) · Journal of Dental Research · doi:10.1177/00220345840630030801 · Cited by 25 · see citing works
Genomic variation in Streptococcus mutans: deletions affecting the multiple pathways of β‐glucoside metabolism
Old, L. A., Lowes, S., & Russell, R. R. B. (2006) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.2005.00246.x · Cited by 22 · cited 2× · see citing works
“Genetic analysis of the cel operon has revealed that cellobiose is internalized by the EIIC permease (celD) and phosphorylated by the activity of EIIA (celC) and EIIB (celB) (111).”
Background
A galactose‐specific sugar: phosphotransferase permease is prevalent in the non‐core genome of S treptococcus mutans
Zeng, L., Xue, P., Stanhope, M. J., & Burne, R. A. (2013) · Molecular Oral Microbiology · doi:10.1111/omi.12025 · Cited by 20 · cited 3× · see citing works
“mutans, particularly when cells are grown in the presence of the sugar(s) that are internalized by these permeases (21, 30, 31).”
Background
Phosphoenolpyruvate-sugar phosphotransferase transport system of Streptococcus mutans: purification of HPr and enzyme I and determination of their intracellular concentrations by rocket immunoelectrophoresis
Thibault, L., & Vadeboncoeur, C. (1985) · Infection and Immunity · doi:10.1128/iai.50.3.817-825.1985 · Cited by 20 · cited 1× · see citing works
“with batch-grown cells (67) and with chemostat cultivated”
Phenotypic stability of the cell wall of Streptococcus mutans Ingbritt grown under various conditions
Knox, K. W., Jacques, N. A., Campbell, L. K., Wicken, A. J., Hurst, S. F., & Bleiweis, A. S. (1979) · Infection and Immunity · doi:10.1128/iai.26.3.1071-1078.1979 · Cited by 20 · see citing works
Concentration-dependent repression of the soluble and membrane components of the Streptococcus mutans phosphoenolpyruvate: sugar phosphotransferase system by glucose
Hamilton, I. R., Gauthier, L., Desjardins, B., & Vadeboncoeur, C. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.6.2942-2948.1989 · Cited by 19 · see citing works
Clustered Genes for Galactose Metabolism from Streptococcus mutans Cloned in Escherichia coli
Smorawinska, M., Hsu, J. C., Hansen, J. B., Jagusztyn-Krynicka, E. K., Abiko, Y., & Curtiss, R. (1983) · Journal of Bacteriology · doi:10.1128/jb.153.2.1095-1097.1983 · Cited by 18 · see citing works
Global control of sugar metabolism: a Gram-positive solution
Titgemeyer, F., & Hillen, W. (2002) · Lactic Acid Bacteria: Genetics, Metabolism and Applications · doi:10.1007/978-94-017-2029-8_4 · Cited by 17 · see citing works
Inhibition of Streptococcus mutans by the antibiotic streptozotocin: mechanisms of uptake and the selection of carbohydrate-negative mutants
Jacobson, G. R., Poy, F., & Lengeler, J. W. (1990) · Infection and Immunity · doi:10.1128/iai.58.2.543-549.1990 · Cited by 16 · cited 1× · see citing works
“mutans through a relatively high-affinity porter as well as through a lower-affinity permease (96), though the identity of these systems was not determined.”
Background
The use of continuous flow bioreactors to explore gene expression and physiology of suspended and adherent populations of oral streptococci
Burne, R. A., & Chen, Y. M. (1998) · Methods in Cell Science · doi:10.1023/a:1009707508738 · Cited by 15 · see citing works
Teflon chemostat for studies of trace metal metabolism in Streptococcus mutans and other bacteria
Strachan, R. C., Aranha, H., Lodge, J., Arceneaux, J. E. L., & Byers, B. R. (1982) · Applied and Environmental Microbiology · doi:10.1128/aem.43.1.257-260.1982 · Cited by 13 · see citing works
The use of continuous flow bioreactors to explore gene expression and physiology of suspended and adherent populations of oral streptococci
Burne, R. A., & Chen, Y. M. (1998) · Springer eBooks · doi:10.1007/978-94-017-2258-2_20 · Cited by 10 · cited 1× · see citing works
“Information on specific aspects of theory and design of continuous culture can be found elsewhere (34, 35).”
Background
Characterization of serological cross-reactivity between polysaccharide antigens of Streptococcus mutans serotypes c and d
Grossi, S. M., Prakobphol, A., Linzer, R., Campbell, L. K., & Knox, K. W. (1983) · Infection and Immunity · doi:10.1128/iai.39.3.1473-1476.1983 · Cited by 7 · see citing works
Characterization of polysaccharide antigens of Streptococcus mutans B13 grown under various conditions
Linzer, R., Campbell, L. K., & Knox, K. W. (1984) · Infection and Immunity · doi:10.1128/iai.44.1.76-81.1984 · Cited by 5 · see citing works

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[79]Bradshaw DJ Lynch RJ Diet and the microbial aetiology of dental caries: new paradigms Int Dent J 2013 63 Suppl 2 64 72 24283286 PMC9375036

Sorted by citations

Oral Biofilms: Pathogens, Matrix, and Polymicrobial Interactions in Microenvironments
Bowen, W. H., Burne, R. A., Wu, H., & Koo, H. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2017.09.008 · Cited by 1,059 · see citing works
“In low-carbohydrate conditions, a pyruvate-formate lyase funnels the pyruvate to acetate and formate, gaining an additional ATP, compared to the lactate pathway [73].”
Background
Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study
Fan, X., Alekseyenko, A. V., Wu, J., Peters, B. A., Jacobs, E. J., Gapstur, S. M., Purdue, M. P., Abnet, C. C., Stolzenberg‐Solomon, R. Z., Miller, G., et al. (2016) · Gut · doi:10.1136/gutjnl-2016-312580 · Cited by 825 · see citing works
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
Dental biofilm: ecological interactions in health and disease
Marsh, P., & Zaura, E. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12679 · Cited by 569 · see citing works
Periodontal Disease: The Good, The Bad, and The Unknown
Sedghi, L. M., Bacino, M. S., & Kapila, Y. L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.766944 · Cited by 385 · see citing works
Oral Microbiome: A Review of Its Impact on Oral and Systemic Health
Krishnamurthy, H. K., Bosco, J., Jayaraman, V., Krishna, K., Wang, T., Bei, K., & Rajasekaran, J. J. (2024) · Microorganisms · doi:10.3390/microorganisms12091797 · Cited by 402 · see citing works
“These microbes drive the development of dental caries-generating acids that erode tooth enamel and initiate cavities [41].”
Background
The Evolving Microbiome of Dental Caries
Spatafora, G., Li, Y., He, X., Cowan, A., & Tanner, A. C. R. (2024) · Microorganisms · doi:10.3390/microorganisms12010121 · Cited by 298 · see citing works
Drinking alcohol is associated with variation in the human oral microbiome in a large study of American adults
Fan, X., Peters, B. A., Jacobs, E. J., Gapstur, S. M., Purdue, M. P., Freedman, N. D., Alekseyenko, A. V., Wu, J., Yang, L., Pei, Z., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0448-x · Cited by 240 · see citing works
Breast tissue, oral and urinary microbiomes in breast cancer
Wang, H., Altemus, J. B., Niazi, F., Green, H., Calhoun, B. C., Sturgis, C. D., Grobmyer, S. R., & Eng, C. (2017) · Oncotarget · doi:10.18632/oncotarget.21490 · Cited by 199 · see citing works
“The relative increase in Streptococcus may be due to the ingestion of carbohydrates [35].”
Background
Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage
Velsko, I. M., Fellows Yates, J. A., Aron, F., Hagan, R. W., Frantz, L. A. F., Loe, L., Martinez, J. B. R., Chaves, E., Gosden, C., Larson, G., et al. (2019) · Microbiome · doi:10.1186/s40168-019-0717-3 · Cited by 170 · see citing works
“Although this species grows prolifically in a laboratory setting and can thrive under a range of environmental conditions [40], it is less common in biofilms from early compared to advanced caries lesions [37–39].”
Background
A Cross-Talk between Diet and the Oral Microbiome: Balance of Nutrition on Inflammation and Immune System’s Response during Periodontitis
Santonocito, S., Giudice, A., Polizzi, A., Troiano, G., Merlo, E. M., Sclafani, R., Grosso, G., & Isola, G. (2022) · Nutrients · doi:10.3390/nu14122426 · Cited by 144 · see citing works
Bacterial Metabolism Shapes the Host–Pathogen Interface
Passalacqua, K. D., Charbonneau, M., & O’Riordan, M. X. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0027-2015 · Cited by 143 · see citing works
“mutans in that it has more levels of carbohydrate catabolite repression flexibility than other Gram-positive bacteria (5, 6).”
Background
Organic Nanomaterials and Their Applications in the Treatment of Oral Diseases
Vîrlan, M. J. R., Miricescu, D., Rădulescu, R., Sabliov, C. M., Totan, A., Calenic, B., & Greabu, M. (2016) · Molecules · doi:10.3390/molecules21020207 · Cited by 114 · see citing works
“Because Streptococcus mutans is one of the most intensively studied cariogenic microorganisms associated with caries progression in humans [51,52], killing this bacterium could be an effective form of preventive dentistry.”
Background
Oral Microbiota Composition Predicts Early Childhood Caries Onset
Grier, A., Myers, J. A., O’Connor, T. G., Quivey, R. G., Gill, S. R., & Kopycka‐Kędzierawski, D. T. (2020) · Journal of Dental Research · doi:10.1177/0022034520979926 · Cited by 101 · see citing works
“which rely on this carbohydrate for their carbon requirements and ability to extract energy from metabolism of sugars (Moye et al. 2014; Baker et al. 2017).”
Background
RNA-Seq Reveals Enhanced Sugar Metabolism in Streptococcus mutans Co-cultured with Candida albicans within Mixed-Species Biofilms
He, J., Kim, D., Zhou, X., Ahn, S., Burne, R. A., Richards, V. P., & Koo, H. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01036 · Cited by 100 · see citing works
“The Frontiers in Microbiology | www.frontiersin.org 8 June 2017 | Volume 8 | Article 1036 galactose moiety of lactose, and possibly galactose alone, can be transported and phosphorylated by a lactose-specific (LacEF) PTS.”
BackgroundInfluential
Therapeutic Strategies Targeting Cariogenic Biofilm Microenvironment
Liu, Y., Ren, Z. F., Hwang, G., & Koo, H. (2018) · Advances in Dental Research · doi:10.1177/0022034517736497 · Cited by 93 · see citing works
Effect of anti-biofilm glass–ionomer cement on Streptococcus mutans biofilms
Wang, S.-P., Ge, Y., Zhou, X.-D., Xu, H. H., Weir, M. D., Zhang, K.-K., Wang, H.-H., Hannig, M., Rupf, S., Li, Q., et al. (2016) · International Journal of Oral Science · doi:10.1038/ijos.2015.55 · Cited by 80 · see citing works
Oral microbiome and obesity in a large study of low-income and African-American populations
Yang, Y., Cai, Q., Zheng, W., Steinwandel, M. D., Blot, W. J., Shu, X., & Long, J. (2019) · Journal of Oral Microbiology · doi:10.1080/20002297.2019.1650597 · Cited by 70 · see citing works
“maintaining oral and systemic health through colonization resistance [10], nutrient digestion [11] and immunity response [12].”
Background
Metabolites 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
Metabolomic profiling of bacterial biofilm: trends, challenges, and an emerging antibiofilm target
Malviya, J., Alameri, A. A., Al-Janabi, S. S., Fawzi, O. F., Azzawi, A. L., Obaid, R. F., Alsudani, A. A., Alkhayyat, A. S., Gupta, J., Mustafa, Y. F., et al. (2023) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-023-03651-y · Cited by 67 · see citing works
Cariogenic Biofilms: Development, Properties, and Biomimetic Preventive Agents
Meyer, F., Enax, J., Epple, M., Amaechi, B. T., & Simader, B. (2021) · Dentistry Journal · doi:10.3390/dj9080088 · Cited by 63 · see citing works
“Glycolysis leads to the metabolism of glucose to adenosine triphosphate (ATP), which is the energy source for the bacteria cell growth and metabolism [63].”
BackgroundInfluential
Polyphenols in Oral Health: Homeostasis Maintenance, Disease Prevention, and Therapeutic Applications
Guo, Y., Li, Z., Chen, F., & Chai, Y. (2023) · Nutrients · doi:10.3390/nu15204384 · Cited by 62 · see citing works
Fluorescent nanosensors reveal dynamic pH gradients during biofilm formation
Hollmann, B., Perkins, M. C., Chauhan, V. M., Aylott, J. W., & Hardie, K. R. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-021-00221-8 · Cited by 60 · see citing works
Genomic and phenotypic diversity of Streptococcus mutans
Bedoya‐Correa, C. M., Rincón‐Rodríguez, R. J., & Parada-Sánchez, M. T. (2018) · Journal of Oral Biosciences · doi:10.1016/j.job.2018.11.001 · Cited by 52 · see citing works
Sucrose- and Fructose-Specific Effects on the Transcriptome of Streptococcus mutans, as Determined by RNA Sequencing
Zeng, L., & Burne, R. A. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.02681-15 · Cited by 50 · see citing works
“Studies by our group have also highlighted the critical role that HPr has on gene regulation, often in cooperation with EIIAB (44).”
BackgroundInfluential
Association between Tooth Loss and Gastric Cancer: A Meta-Analysis of Observational Studies
Yin, X., Wang, Y., Luo, H. L., Zhao, K., Huang, G., Luo, S., Peng, J., & Song, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149653 · Cited by 50 · see citing works
A GntR Family Transcription Factor in Streptococcus mutans Regulates Biofilm Formation and Expression of Multiple Sugar Transporter Genes
Li, Z., Xiang, Z., Zeng, J., Li, Y., & Li, J. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03224 · Cited by 49 · see citing works
Salivary microbiome and metabolome analysis of severe early childhood caries
Li, K., Wang, J., Du, N., Sun, Y., Sun, Q., Yin, W., Li, H., Meng, L., & Liu, X. (2023) · BMC Oral Health · doi:10.1186/s12903-023-02722-8 · Cited by 48 · see citing works
“During caries development, excess carbohydrate levels can alter the local microenvironment and contribute to caries induction by related bacteria such as Streptococcus mutans [63].”
Background
Streptococcus mutans Displays Altered Stress Responses While Enhancing Biofilm Formation by Lactobacillus casei in Mixed-Species Consortium
Wen, Z. T., Liao, S., Bitoun, J. P., De, A., Jorgensen, A. N., Feng, S., Xu, X., Chain, P., Caufield, P. W., Koo, H., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00524 · Cited by 45 · see citing works
Association of the Microbiota and Pancreatic Cancer: Opportunities and Limitations
Chen, Z., Zhang, S., Dong, S., Xu, H. M., & Zhou, W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.844401 · Cited by 45 · see citing works
Coordinated Regulation of the EII Man and fruRKI Operons of Streptococcus mutans by Global and Fructose-Specific Pathways
Zeng, L., Chakraborty, B., Farivar, T., & Burne, R. A. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01403-17 · Cited by 44 · see citing works
“mutans are often capable of transporting multiple substrates with various degrees of specificity (3).”
Background
Dietary carbohydrate intake is associated with the subgingival plaque oral microbiome abundance and diversity in a cohort of postmenopausal women
Millen, A. E., Dahhan, R., Freudenheim, J. L., Hovey, K. M., Li, L., McSkimming, D. I., Andrews, C., Buck, M. J., LaMonte, M. J., Kirkwood, K. L., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-06421-2 · Cited by 41 · see citing works
Meta‐analysis of caries microbiome studies can improve upon disease prediction outcomes
Butcher, M., Short, B., Veena, C. L. R., Bradshaw, D., Pratten, J., McLean, W., Shaban, S., Ramage, G., & Delaney, C. (2022) · Acta Pathologica, Microbiologica et Immunologica Scandinavica (APMIS) · doi:10.1111/apm.13272 · Cited by 26 · see citing works
“04), both key processes in fuelling carbohydrate metabolism (33,34).”
Background
Oral Microbiota: The Influences and Interactions of Saliva, IgA, and Dietary Factors in Health and Disease
Nagakubo, D., & Kaibori, Y. (2023) · Microorganisms · doi:10.3390/microorganisms11092307 · Cited by 69 · see citing works
“Meals serve as a source of nutrition for oral bacteria, and the nutrients consumed can inﬂuence the selection of bacteria that can survive in the oral cavity [86].”
Background
Addition of cariogenic pathogens to complex oral microflora drives significant changes in biofilm compositions and functionalities
Liu, Y., Daniel, S. G., Kim, H., Koo, H., Korostoff, J. M., Teles, F., Bittinger, K. L., & Hwang, G. (2023) · Microbiome · doi:10.1186/s40168-023-01561-7 · Cited by 41 · see citing works
Manipulating the diseased oral microbiome: the power of probiotics and prebiotics
Yu, X., DeVine, D., & Vernon, J. J. (2024) · Journal of Oral Microbiology · doi:10.1080/20002297.2024.2307416 · Cited by 40 · see citing works
“Cariogenic bacteria in dental plaque, such as Streptococcus mutans , metabolise fer-mentable dietary carbohydrates producing acid, which decreases pH and causes enamel demineralization over time [72,73].”
Background
CcpA-Dependent Carbon Catabolite Repression Regulates Fructooligosaccharides Metabolism in Lactobacillus plantarum
Chen, C., Lu, Y., Wang, L., Yu, H., & Tian, H. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01114 · Cited by 38 · see citing works
“During these regulatory processes, CcpA plays a central role that inactivation the ccpA gene leads to partial or complete relief of CCR (Moye et al., 2014; Zeng et al., 2017).”
Background
Genetic polymorphisms of the sortase A gene and social-behavioural factors associated with caries in children: a case–control study
Yu, L. X., Tao, Y., Qiu, R. M., Zhou, Y. N., Zhi, Q. H., & Lin, H. (2015) · BMC Oral Health · doi:10.1186/s12903-015-0039-1 · Cited by 37 · see citing works
“mutans to produce the plaque dextrans essential for acid production [27].”
Background
Effects of Carbohydrate Source on Genetic Competence in Streptococcus mutans
Moye, Z. D., Son, M., Rosa-Alberty, A. E., Zeng, L., Ahn, S., Hagen, S. J., & Burne, R. A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01205-16 · Cited by 36 · see citing works
“mutans (37), loss of CcpA did have a significant 473 impact on the response of this organism to CSP in the sugars tested.”
Background
Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage
Wei, L., Yang, J., Ahmed, W., Xiong, X., Liu, Q., Huang, Q., & Ji, G. (2021) · Agronomy · doi:10.3390/agronomy11122424 · Cited by 33 · see citing works
Dental caries: Genetic and protein interactions
Cavallari, T., Arima, L. Y., Ferrasa, A., Moysés, S. J., Moysés, S. T., Herai, R. H., & Werneck, R. I. (2019) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2019.104522 · Cited by 32 · see citing works
EpsR Negatively Regulates Streptococcus mutans Exopolysaccharide Synthesis
Chen, J., Zhang, A., Xiang, Z., Lu, M., Huang, P., Gong, T., Pan, Y., Lin, Y., Zhou, X., & Li, Y. (2021) · Journal of Dental Research · doi:10.1177/00220345211000668 · Cited by 32 · see citing works
“PTS system sugar transporters can monitor the type and levels of carbohydrates present in the oral cavity (Moye et al. 2014).”
Background
Taxonomic and functional alterations in the salivary microbiota of children with and without severe early childhood caries (S-ECC) at the age of 3
Tang, Z., Xu, W., Zhou, Z., Qiao, Y., Zheng, S., & Rong, W. (2022) · PeerJ · doi:10.7717/peerj.13529 · Cited by 31 · see citing works
Dietary Nitrite Drives Disease Outcomes in Oral Polymicrobial Infections
Scoffield, J. A., Michalek, S. M., Harber, G. J., Eipers, P. G., Morrow, C. D., & Wu, H. (2019) · Journal of Dental Research · doi:10.1177/0022034519855348 · Cited by 31 · see citing works
On the Pathogenicity of the Oral Biofilm: A Critical Review from a Biological, Evolutionary, and Nutritional Point of View
Woelber, J. P., Al‐Ahmad, A., & Alt, K. W. (2022) · Nutrients · doi:10.3390/nu14102174 · Cited by 34 · see citing works
“, respiration and fermentation) [34] depending on the environmental factors so that nutrition, oxygen, and pH-value increases the adaptation capacity of oral biofilm.”
Background
CcpA and CodY Coordinate Acetate Metabolism in Streptococcus mutans
Kim, J. N., & Burne, R. A. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.03274-16 · Cited by 31 · see citing works
“mutans alleviates catabolite repression (17).”
Modification of the Streptococcus mutans transcriptome by LrgAB and environmental stressors
Rice, K. C., Turner, M. E., Carney, O. O., Gu, T., & Ahn, S. (2016) · Microbial Genomics · doi:10.1099/mgen.0.000104 · Cited by 30 · see citing works
“These include competition for nutrients and physical real estate within dental plaque biofilm, as well as adaptation to fluxes in environmental pH, temperature and oxidative stress (reviewed in [2, 3]).”
The European Association for Sports Dentistry, Academy for Sports Dentistry, European College of Sports and Exercise Physicians consensus statement on sports dentistry integration in sports medicine
Stamos, A., Mills, S., Malliaropoulos, N., Cantamessa, S., Dartevelle, J., Gündüz, E., Laubmeier, J., Hoy, J., Kakavas, G., Garrec, S. L., et al. (2020) · Dental Traumatology · doi:10.1111/edt.12593 · Cited by 40 · see citing works
Matrix Dynamics and Microbiome Crosstalk: Matrix Metalloproteinases as Key Players in Disease and Therapy
Ioannou, P., Katsoulieris, E. N., & Afratis, N. A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26083621 · Cited by 33 · see citing works
Effect of divalent ions on cariogenic biofilm formation
Steiger, E., Muelli, J., Braissant, O., Waltimo, T. M. T., & Astasov‐Frauenhoffer, M. (2020) · BMC Microbiology · doi:10.1186/s12866-020-01973-7 · Cited by 29 · see citing works
“high numbers of Streptococcus mutans [14, 15].”
Bacteria associated with human saliva are major microbial components of Ecuadorian indigenous beers ( chicha )
Freire, A. L., Zapata, S., Mosquera, J. D., Mejía, L., & Trueba, G. A. (2016) · PeerJ · doi:10.7717/peerj.1962 · Cited by 28 · see citing works
Antibacterial potency and fluoride release of a glass ionomer restorative material containing different concentrations of natural and chemical products: An in-vitro comparative study
Elgamily, H. M., Ghallab, O. H., El-Sayed, H. S., & Nasr, M. (2018) · Journal of Clinical and Experimental Dentistry · doi:10.4317/jced.54606 · Cited by 28 · see citing works
“mutans is a solitary bacterial biofilm and has been utilized as a part of a few past investigations of antibacterial dental materials as a result of its involvement with dental caries (33-36).”
Background
Molecular mechanisms controlling fructose‐specific memory and catabolite repression in lactose metabolism by Streptococcus mutans
Zeng, L., & Burne, R. A. (2020) · Molecular Microbiology · doi:10.1111/mmi.14597 · Cited by 27 · see citing works
“In vitro phosphorylation of glucose via glucokinase (Sato et al., 2015) or the PTS (Moye et al., 2014a) was performed according to established protocols.”
BackgroundMethod
Transcriptional Activity of Predominant Streptococcus Species at Multiple Oral Sites Associate With Periodontal Status
Belstrøm, D., Constancias, F., Markvart, M., Sikora, M., Sørensen, C. E., & Givskov, M. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.752664 · Cited by 27 · see citing works
Influence of 2′-fucosyllactose and galacto-oligosaccharides on the growth and adhesion of Streptococcus mutans
Salli, K. M., Söderling, E. M., Hirvonen, J., Gürsoy, U. K., & Ouwehand, A. C. (2020) · British Journal Of Nutrition · doi:10.1017/s0007114520001956 · Cited by 25 · see citing works
“mutans is well adapted to thrive in the oral cavity and canmetabolise many carbon sources(11,23,31,32).”
Background
Effects of glucose and lactate on Streptococcus mutans abundance in a novel multispecies oral biofilm model
Sangha, J. S., Barrett, P., Curtis, T. P., Métris, A., Jakubovics, N. S., & Ofiţeru, I. D. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.03713-23 · Cited by 24 · see citing works
“…growth experiments, the AFMC medium was supplemented with 20 g L −1 glucose as the preferred primary carbon source for S. gordonii , S. mutans , A. oris , and N. subflava (24, 25) and 12.1 g L −1 lactic acid, as the primary carbon source for V. parvula , which cannot metabolize glucose (26).”
MethodInfluential
Mediterranean diet: a potential player in the link between oral microbiome and oral diseases
Augimeri, G., Caparello, G., Caputo, I., Reda, R., Testarelli, L., & Bonofiglio, D. (2024) · Journal of Oral Microbiology · doi:10.1080/20002297.2024.2329474 · Cited by 23 · see citing works
Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species
Mann, A. E., Chakraborty, B., O’Connell, L. M., Nascimento, M. M., Burne, R. A., & Richards, V. P. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.01445-23 · Cited by 22 · see citing works
“We also find multiple Streptococcus mutans genes upregulated in the disease, which are key factors in carbohydrate metabolism, including ccp A, cod Y, pac L, gtf A, gtf C, lev D, and fru A (47, 48).”
Background
Analysis of cariogenic potential of alternative milk beverages by in vitro Streptococcus mutans biofilm model and ex vivo caries model
Huang, Y., Thompson, T., Wang, Y., Yu, Q., Zhu, L. D., Xu, X., Wen, Z. T., & Townsend, J. A. (2019) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2019.05.033 · Cited by 22 · see citing works
Bacterial Metabolism Shapes the Host-Pathogen Interface
Passalacqua, K. D., Charbonneau, M., & O’Riordan, M. X. (2016) · ASM Press eBooks · doi:10.1128/9781555819286.ch2 · Cited by 21 · see citing works
Characterization of the pgf operon involved in the posttranslational modification of Streptococcus mutans surface proteins
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Glucose Phosphotransferase System Modulates Pyruvate Metabolism, Bacterial Fitness, and Microbial Ecology in Oral Streptococci
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“Although the disease is associated with specific bacteria (Streptococcus mutans and Lactobacillus) that exist as part of the normal flora of the oral cavity, the increased consumption of carbohydrates may have been a significant force behind its wide-reaching global spread (Moye et al., 2014).”
Amino Sugars Reshape Interactions between Streptococcus mutans and Streptococcus gordonii
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“…have broadened understanding of the diversity of bacteria present in the oral cavity, with estimates ranging from 600 to >1200 different microbial taxa (Moye et al. 2014) and the balance between the health- and caries-associated flora may also play a role in the severity of dental caries.”
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Lactobacillus rhamnosus GG in Experimental Oral Biofilms Exposed to Different Carbohydrate Sources
Jiang, Q., Kainulainen, V., Stamatova, I., Korpela, R., & Meurman, J. H. (2018) · Caries Research · doi:10.1159/000479380 · Cited by 18 · see citing works
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A Membrane-Targeted Peptide Inhibiting PtxA of Phosphotransferase System Blocks Streptococcus mutans
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“mutans encodes as many as 15 different EII permeases, composed of A, B, C, and occasionally D, domains [Moye et al., 2014].”
Background
Chronic fatigue syndrome patients have alterations in their oral microbiome composition and function
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Fewer Children in Families Associated with Lower Odds of Early Childhood Caries: A Sample from Three Countries
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“These enzymes catalyze synthesis of glucans from sucrose [42].”
Background
Novel Lactotransferrin-Derived Antimicrobial Peptide LF-1 Inhibits the Cariogenic Virulence Factors of Streptococcus mutans
Luo, J., Feng, Z., Lyu, X., & Zhang, L. (2023) · Antibiotics · doi:10.3390/antibiotics12030563 · Cited by 14 · see citing works
“mutans carbohydrate metabolism that generates acidic by-products [23].”
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High conservation of the dental plaque microbiome across populations with differing subsistence strategies and levels of market integration
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“Dental plaque microbiomes of USE populations are notably different between healthy teeth and those experiencing dental disease, particularly dental caries or periodontal disease (Nascimento et al., 2017 ; Socransky & Haffajee, 2005).”
Low Carbohydrate, High Fat Diet Alters the Oral Microbiome without Negating the Nitrite Response to Beetroot Juice Supplementation
Cato, L. E., McKay, A. K. A., L’Heureux, J. E., Vanhatalo, A., JONES, A. M., Askew, C. D., Slater, G., & Burke, L. M. (2023) · Nutrients · doi:10.3390/nu15245123 · Cited by 14 · see citing works
“A higher intake of dietary carbohydrate favours key carbohydrate metabolising bacterial species, including Streptococcus mutans [50].”
Background
Efficient biocatalytic synthesis of D-tagatose 1,6-diphosphate by LacC-catalysed phosphorylation of D-tagatose 6-phosphate
Schoenenberger, B., Kind, S., Meier, R., Eggert, T., Obkircher, M., & Wohlgemuth, R. (2019) · Biocatalysis and Biotransformation · doi:10.1080/10242422.2019.1634694 · Cited by 13 · see citing works
“…as metabolite standard in metabolomics, but also in the investigation of critically important roles of tagatose pathways in pathogenic bacteria, e.g. in lactose and galactose utilization by the cariogenic oral bacterium S. mutans (Hamilton and Lebtag 1979; Abranches et al. 2004; Moye et al. 2014).”
Background
Guanidine hydrochloride polymer additive to undertake ultraconservative resin infiltrant against Streptococcus mutans
Collares, F. M., García, I. M., Bohns, F. R., da Motta, A. D. S., Melo, M. A. S., & Leitune, V. C. B. (2020) · European Polymer Journal · doi:10.1016/j.eurpolymj.2020.109746 · Cited by 13 · see citing works
The Impact of Diet and Nutrition on the Oral Microbiome
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Carbon source utilization patterns in dental plaque and microbial responses to sucrose, lactose, and phenylalanine consumption in severe early childhood caries
Shi, W., Tian, J., Xu, H., Wang, G., Zhou, Q., & Qin, M. (2020) · Journal of Oral Microbiology · doi:10.1080/20002297.2020.1782696 · Cited by 12 · see citing works
“mutans had evolved elegant strategies to cope with the different carbohydrates present within the oral cavity [10].”
Background
Temporal dynamics and composition of ocular surface microbiota in C57BL/6J mice: uncovering a 12h ultradian rhythm
Jiao, X., & Li, Z. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1244454 · Cited by 11 · see citing works
“This dynamic property allows the microbiota to adapt to environmental changes and anticipate ﬂ uctuating physiological demands of the host (Moye et al., 2014; Jehrke et al., 2018; Gomez-Alvarez et al., 2021).”
Background
Associations between self-reported psychological symptom severity and gut microbiota: further support for the microgenderome
Ganci, M., Suleyman, E., Butt, H., & Ball, M. (2022) · BMC Psychiatry · doi:10.1186/s12888-022-03947-7 · Cited by 11 · see citing works
Antibodies generated against dextransucrase exhibit potential anticariostatic properties in Streptococcus mutans
Rather, S. A., Sharma, S. C., & Mahmood, A. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10327-x · Cited by 11 · see citing works
Interplay between dental caries pathogens, periodontal pathogens, and sugar molecules: approaches for prevention and treatment
Ealla, K. K. R., Kumari, N., Chintalapani, S., Uppu, S., Sahu, V., Veeraraghavan, V. P., Ramani, P., & Govindool, S. R. (2024) · Archives of Microbiology · doi:10.1007/s00203-024-03856-1 · Cited by 10 · see citing works
“Several studies have shown the role of different sugars, such as sucrose, glucose, galactose, erythritol, xylitol, and D -tagatose in dental caries and periodontal disease (Jin et al. 2004; Moye et al. 2014; Jakubovics 2015; Martinon et al. 2021).”
Influential
Engineering D-glucose utilization in Azospirillum brasilense Sp7 promotes rice root colonization
Singh, V. S., Dubey, B. K., Rai, S., Singh, S. P., & Tripathi, A. K. (2022) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-022-12250-0 · Cited by 10 · see citing works
“Usually, NAG is transported via a NagE transporter, phosphorylated, and then deacetylated by N-acetylglucosamine-6-phosphate deacetylase (NagA) to produce glucosamine-6-phosphate, which is then converted into fructose-6-phosphate by glucosamine-6-phosphate deaminase (NagB) or glucosaminefructose-6-phosphate aminotrans…”
BackgroundInfluential
Manganese transport by Streptococcus sanguinis in acidic conditions and its impact on growth in vitro and in vivo
Puccio, T., An, S., Schultz, A. C., Lizarraga, C. A., Bryant, A. S., Culp, D. J., Burne, R. A., & Kitten, T. O. (2021) · Molecular Microbiology · doi:10.1111/mmi.14854 · Cited by 9 · see citing works
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“Chitosan”
Background
The fruB Gene of Streptococcus mutans Encodes an Endo-Levanase That Enhances Growth on Levan and Influences Global Gene Expression
Chakraborty, B., Zeng, L., & Burne, R. A. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00522-22 · Cited by 9 · see citing works
Genetic diversity of Streptococcus mutans serotype c isolated from white spot and cavitated caries lesions from schoolchildren
Rincón‐Rodríguez, R. J., Parada-Sánchez, M. T., Bedoya‐Correa, C. M., & Toro, D. A. (2019) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2019.02.003 · Cited by 9 · see citing works
The Plaque Microbiota Community of Giant Panda (Ailuropoda melanoleuca) Cubs With Dental Caries
Ma, R., Hou, R., Guo, J.-L., Zhang, X., Cao, S., Huang, X.-B., Wu, R. T., Wen, Y., Zhao, Q., Du, S., et al. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.866410 · Cited by 9 · see citing works
“As with most previously reported findings, enhanced metabolic pathways are positively associated with the development of caries, especially carbohydrate metabolism (Moye et al., 2014; Strużycka, 2014; Wang et al., 2019).”
Background
Insight into the Effect of Small RNA srn225147 on Mutacin IV in Streptococcus mutans
Liu, S., Li, H., Guo, Z., Guan, J.-C., Sun, Y., & Zhang, K. (2019) · Indian Journal of Microbiology · doi:10.1007/s12088-019-00820-2 · Cited by 9 · see citing works
Dental Calculus Formation Rate: The Role of Salivary Proteome and Metaproteome
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“Surplus carbohydrates in the oral environment foster conditions favourable to pathogenic bacteria associated with oral diseases (Moye et al. 2014).”
Effects of graphene oxide and graphene quantum dots on enhancing CPP-ACP anti-caries ability of enamel lesion in a biofilm-challenged environment
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Streptococcus mutans and Cariogenic Biofilms: Mechanisms, Disruption Strategies, and Future Therapeutic Directions
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Adaptive metabolic strategies of intracellular bacterial pathogens
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“Metabolic flexibility has significantly influenced the evolutionary dynamics between pathogens and their human hosts (Moye et al., 2014).”
A Docking and Network Pharmacology Study on the Molecular Mechanisms of Curcumin in Dental Caries and Streptococcus mutans
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Effect of Different Glucose Concentrations on Small RNA Levels and Adherence of Streptococcus mutans
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Background

REVIEW ARTICLE Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans
Moye, Z. D., Zeng, L., & Burne, R. A. (2016)
Streptococcus mutans and its ability to metabolize various carbohydrates
Pašková, K., Linhartová, P. B., Kučera, J., Řemínek, R., Zapletalová, M., Lochman, J., & Hollá, L. I. (2017)
Gene Regulation in S. mutans
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Streptococcus mutans, an assessment of its physiological potential in relation to dental caries.
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Carbohydrate source effects on the transcriptome of Streptococcus mutans
Zapletalová, M., Pašková, K., Kučera, J., Lochman, J., & Linhartová, P. B. (2018)

Authors: Moye, Z. D., Zeng, L., & Burne, R. A.
Affiliations: University of Florida (US)
Corresponding author: Burne, Robert A.
ORCID: Moye, Zachary D.
Zeng, Lin
Burne, Robert A.
Venue: Journal of Oral Microbiology
Publisher: Informa UK Limited
Published: 2014-01-01
Volume: 6
Issue: 1
Pages: 24878
ISSN: 2000-2297 (ISSN-L)
DOI: 10.3402/jom.v6.24878
PMC: PMC4157138
OpenAlex: W2100691159
Cited by: 164
References: 142
Citations by year: 2026: 13 · 2025: 17 · 2024: 17 · 2023: 17 · 2022: 19 · 2021: 13 · 2020: 15 · 2019: 10 · 2018: 12 · 2017: 10 · 2016: 15 · 2015: 5 · 2014: 1
FWCI: 1.74
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
Locations: Journal of Oral Microbiology (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: National Institute of Allergy and Infectious Diseases (T32AI007110)
National Institute of Dental and Craniofacial Research (DE12236, R01DE019783, T90DE021990, R01DE012236)
Topics: Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Health Sciences › Dentistry › Periodontics › Dental Health and Care Utilization
Keywords: Streptococcus mutans, dental caries, carbohydrate metabolism, gene expression regulation, oral microbiota, chemostat cultivation, nutrient acquisition, bacterial pathogenicity, host-pathogen interaction, carbohydrate catabolism

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Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans

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