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Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans
Open accessAbstract
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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![Fig. 1 S. mutans has evolved elegant strategies for coping with the diversity and availability of nutrients present within the oral cavity. When a preferred carbohydrate source, such as glucose, is present in abundant quantities, the elevated movement of metabolites through glycolysis profoundly alters many cellular properties. For instance, the kinase activity of the HPr kinase/phosphatase (HprK) is stimulated leading to an increase in the serine-phosphorylated species of HPr [HPr(Ser-P)]. HPr(Ser-P) acts as a co-factor of the major regulator CcpA to repress transcription of metabolic genes containing a catabolite response element (CRE) in their promoter regions, or in the cases of CcpA-independent CCR, directly affects transcription of genes associated with catabolism of non-preferred carbohydrate sources, a process that may also require certain PTS permeases. As the supply of available carbohydrate is diminished, the reduced quantity of readily metabolizable carbohydrate translates to a lower abundance of HPr(Ser-P). Without its co-factor, CcpA no longer functions as a repressor, and with lower levels of carbohydrate transport occurring, PTS porters remain predominately phosphorylated and play a less active role in CCR. Relief of repression by these factors allows for transcription of a variety of genes, including PTS porters, for sensing and accessing a diverse array of carbohydrate sources. Overall, PTS porters monitor the type and levels of carbohydrates present in the oral cavity, while the overall supply of carbohydrate in relation to cellular energy demands is monitored by the activity of HPr and CcpA.](/paper-figures/0bab60f8f4414040a73f106555b1a67d/fueling-the-caries-process-carbohydrate-metabolism-and-gene-regulation-by-i-figure-1.jpg)
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“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“Saccharolytic bacteria, including Streptococcus, Actinomyces, and Veillonella species, degrade carbohydrates via the Embden‐Meyerhof‐Parnas pathways to produce acidic by‐products, including lactate, acetate, ethanol, and formate, which cause demineralization of dental enamel and the development of carious lesions.”
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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“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).”
BackgroundInfluentialPneumococcal 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×
“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).”
BackgroundCharacterization 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×
“mutans produces a secreted exob-D-fructosidase, FruA, that releases fructose from b2, 6 and b2,1-linked fructan polymers (88, 89).”
BackgroundUptake 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×
“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).”
BackgroundInfluentialEnvironmental 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 73 · cited 1×
“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).”
BackgroundCcpA 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×
“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).”
BackgroundPTS 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×
“pyogenes possesses a CcpAbinding site upstream of the promoter for mga (130, 131).”
BackgroundTranscriptional 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×
“Likewise, deletion of EIIB was thought to cause constitutive phosphorylation of EIIA, leading to inactivation of CelR (24).”
BackgroundInfluentialDifferential 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 71 · cited 1×
“mutans due to the presence of a highaffinity galactose PTS, a trait that may help to promote dental health (108, 109).”
BackgroundTransport 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×
“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).”
BackgroundGene 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×
“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).”
ResultZeng, L., & Burne, R. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.07029.x · Cited by 67 · cited 1×
“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).”
BackgroundUtilization 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×
“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).”
BackgroundZeng, L., & Burne, R. A. (2012) · Journal of Bacteriology · doi:10.1128/jb.02042-12 · Cited by 63 · cited 4×
“mutans, particularly when cells are grown in the presence of the sugar(s) that are internalized by these permeases (21, 30, 31).”
BackgroundInfluentialJacques, 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
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
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×
“which is active in PTS-deficient cells (66), it is likely that”
BackgroundDerr, 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×
“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).”
BackgroundMcKessar, S. J., & Hakenbeck, R. (2007) · Journal of Bacteriology · doi:10.1128/jb.01170-06 · Cited by 58 · cited 1×
“mutans and Streptococcus pneumoniae is necessary for the efficient internalization of cellobiose (23, 24).”
BackgroundAn 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×
“coli and other members of Enterobacteriaceae (103, 104), or by a metabolitebinding ribozyme in many Gram-positive organisms (105, 106).”
BackgroundGöpel, 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×
“coli and other members of Enterobacteriaceae (103, 104), or by a metabolitebinding ribozyme in many Gram-positive organisms (105, 106).”
BackgroundHamilton, 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×
“stores (65), closely resembling previous results (46).”
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
Henstra, S. A., Duurkens, R. H., & Robillard, G. T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.10.7037 · Cited by 55
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
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×
“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.”
BackgroundVadeboncoeur, C., Brochu, D., & Reizer, J. (1991) · Analytical Biochemistry · doi:10.1016/0003-2697(91)90112-7 · Cited by 53 · cited 1×
“been noted with batch-grown cells (68).”
Hamilton, I. R., & Bowden, G. H. W. (1982) · Infection and Immunity · doi:10.1128/iai.36.1.255-262.1982 · Cited by 53
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×
“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).”
BackgroundThe 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
Zeng, L., & Burne, R. A. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06403.x · Cited by 51 · cited 3×
“In particular, CcpA has the ability to indirectly influence non-preferred sugar uptake by regulating the expression of multiple EII permeases (31).”
BackgroundCellular 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×
“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).”
BackgroundMoye, Z. D., Zeng, L., & Burne, R. A. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03579-13 · Cited by 50 · cited 6×
“and excess carbohydrate conditions (65), and these”
BackgroundMethodInfluentialEffect 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
Homer, K. A., Patel, R., & Beighton, D. (1993) · Infection and Immunity · doi:10.1128/iai.61.1.295-302.1993 · Cited by 46
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×
“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).”
BackgroundJacques, 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
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
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×
“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).”
BackgroundWENHAM, D. G., Hennessey, T. D., & Cole, J. A. (1979) · Journal of General Microbiology · doi:10.1099/00221287-114-1-117 · Cited by 37
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
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×
“mutans due to the presence of a highaffinity galactose PTS, a trait that may help to promote dental health (108, 109).”
BackgroundVadeboncoeur, 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
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×
“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).”
BackgroundSucrose, the arch criminal of dental caries.
Newbrun, E. (1969) · PubMed · Cited by 33
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×
“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).”
BackgroundResultEllwood, D. C., & Hamilton, I. R. (1982) · Infection and Immunity · doi:10.1128/iai.36.2.576-581.1982 · Cited by 30
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
Bouraoui, H., Ventroux, M., Noirot‐Gros, M., Deutscher, J., & Joyet, P. (2012) · Molecular Microbiology · doi:10.1111/mmi.12131 · Cited by 29 · cited 1×
“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.”
BackgroundKietzman, C. C., & Caparon, M. G. (2010) · Infection and Immunity · doi:10.1128/iai.01026-10 · Cited by 29 · cited 1×
“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).”
BackgroundPoy, F., & Jacobson, G. R. (1990) · Infection and Immunity · doi:10.1128/iai.58.5.1479-1480.1990 · Cited by 28 · cited 1×
“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).”
BackgroundGera, 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×
“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.”
MethodBiochemical 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×
“mutans from the related cariogenic species Streptococcus sobrinus (94, 95).”
BackgroundAjdić, D., & Chen, Z. (2012) · Molecular Oral Microbiology · doi:10.1111/omi.12009 · Cited by 26 · cited 4×
“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.”
BackgroundInfluentialRodrigue, L., Lacoste, L., Trahan, L., & Vadeboncoeur, C. (1988) · Infection and Immunity · doi:10.1128/iai.56.2.518-522.1988 · Cited by 25
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×
“mutans, and this benefit required the presence of an intact tagatose pathway (110), which is a primary route for galactose catabolism in S.”
BackgroundActivity 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
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×
“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).”
BackgroundZeng, L., Xue, P., Stanhope, M. J., & Burne, R. A. (2013) · Molecular Oral Microbiology · doi:10.1111/omi.12025 · Cited by 20 · cited 3×
“mutans, particularly when cells are grown in the presence of the sugar(s) that are internalized by these permeases (21, 30, 31).”
BackgroundThibault, L., & Vadeboncoeur, C. (1985) · Infection and Immunity · doi:10.1128/iai.50.3.817-825.1985 · Cited by 20 · cited 1×
“with batch-grown cells (67) and with chemostat cultivated”
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
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
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
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
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×
“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.”
BackgroundBurne, R. A., & Chen, Y. M. (1998) · Methods in Cell Science · doi:10.1023/a:1009707508738 · Cited by 15
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
Burne, R. A., & Chen, Y. M. (1998) · Springer eBooks · doi:10.1007/978-94-017-2258-2_20 · Cited by 10 · cited 1×
“Information on specific aspects of theory and design of continuous culture can be found elsewhere (34, 35).”
BackgroundGrossi, 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
Linzer, R., Campbell, L. K., & Knox, K. W. (1984) · Infection and Immunity · doi:10.1128/iai.44.1.76-81.1984 · Cited by 5
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Metadata
- Authors
- Moye, Z. D., Zeng, L., & Burne, R. A.
- Affiliations
- University of Florida (US)
- Corresponding author
- 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)
- 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 › General Dentistry › 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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