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Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during biofilm development.

Klein MI, DeBaz L, Agidi S, Lee H, Xie G, Lin AH, Hamaker BR, Lemos JA, Koo H - PLoS ONE (2010)

Bottom Line: Overall, the presence of sucrose and starch (suc+st) influenced the dynamics of S. mutans transcriptome (vs. sucrose alone), which may be associated with gradual digestion of starch by surface-adsorbed amylase.In contrast, at 30 h of biofilm development, multiple genes associated with sugar uptake/transport (e.g. maltose), two-component systems, fermentation/glycolysis and iron transport were differentially expressed in suc+st-biofilms (vs. sucrose-biofilms).Our data show complex remodeling of S. mutans-transcriptome in response to changing environmental conditions in situ, which could modulate the dynamics of biofilm development and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Center for Oral Biology and Eastman Department of Dentistry, University of Rochester Medical Center, Rochester, New York, United States of America.

ABSTRACT
The combination of sucrose and starch in the presence of surface-adsorbed salivary α-amylase and bacterial glucosyltransferases increase the formation of a structurally and metabolically distinctive biofilm by Streptococcus mutans. This host-pathogen-diet interaction may modulate the formation of pathogenic biofilms related to dental caries disease. We conducted a comprehensive study to further investigate the influence of the dietary carbohydrates on S. mutans-transcriptome at distinct stages of biofilm development using whole genomic profiling with a new computational tool (MDV) for data mining. S. mutans UA159 biofilms were formed on amylase-active saliva coated hydroxyapatite discs in the presence of various concentrations of sucrose alone (ranging from 0.25 to 5% w/v) or in combination with starch (0.5 to 1% w/v). Overall, the presence of sucrose and starch (suc+st) influenced the dynamics of S. mutans transcriptome (vs. sucrose alone), which may be associated with gradual digestion of starch by surface-adsorbed amylase. At 21 h of biofilm formation, most of the differentially expressed genes were related to sugar metabolism, such as upregulation of genes involved in maltose/maltotriose uptake and glycogen synthesis. In addition, the groEL/groES chaperones were induced in the suc+st-biofilm, indicating that presence of starch hydrolysates may cause environmental stress. In contrast, at 30 h of biofilm development, multiple genes associated with sugar uptake/transport (e.g. maltose), two-component systems, fermentation/glycolysis and iron transport were differentially expressed in suc+st-biofilms (vs. sucrose-biofilms). Interestingly, lytT (bacteria autolysis) was upregulated, which was correlated with presence of extracellular DNA in the matrix of suc+st-biofilms. Specific genes related to carbohydrate uptake and glycogen metabolism were detected in suc+st-biofilms in more than one time point, indicating an association between presence of starch hydrolysates and intracellular polysaccharide storage. Our data show complex remodeling of S. mutans-transcriptome in response to changing environmental conditions in situ, which could modulate the dynamics of biofilm development and pathogenicity.

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Amounts of intracellular polysaccharides (IPS) in the biofilms.Total amounts of IPS in mg/mg of biofilm dry-weight. The data sh own are mean values (±SD; n = 9) from three independent experiments. Values with an asterisk (*) are significantly different from other group (P<0.05, ANOVA comparison for all pairs using Tukey test); suc+st −0.5% sucrose +1% starch, and suc−1% sucrose.
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pone-0013478-g006: Amounts of intracellular polysaccharides (IPS) in the biofilms.Total amounts of IPS in mg/mg of biofilm dry-weight. The data sh own are mean values (±SD; n = 9) from three independent experiments. Values with an asterisk (*) are significantly different from other group (P<0.05, ANOVA comparison for all pairs using Tukey test); suc+st −0.5% sucrose +1% starch, and suc−1% sucrose.

Mentions: The expression of gene glg (which encodes a glycogen phosphorylase) was enhanced in biofilms formed in the presence of sucrose plus starch at 21 h and 24 h (vs. suc-biofilms; see Data S3) which could reflect in changes on IPS metabolism during the biofilms development process. Indeed, the determination of the IPS content revealed that suc+st-biofilms at 30 h of biofilm growth have significantly higher amounts of IPS compared to biofilms formed in sucrose alone (P<0.05) (Fig.6).


Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during biofilm development.

Klein MI, DeBaz L, Agidi S, Lee H, Xie G, Lin AH, Hamaker BR, Lemos JA, Koo H - PLoS ONE (2010)

Amounts of intracellular polysaccharides (IPS) in the biofilms.Total amounts of IPS in mg/mg of biofilm dry-weight. The data sh own are mean values (±SD; n = 9) from three independent experiments. Values with an asterisk (*) are significantly different from other group (P<0.05, ANOVA comparison for all pairs using Tukey test); suc+st −0.5% sucrose +1% starch, and suc−1% sucrose.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2957427&req=5

pone-0013478-g006: Amounts of intracellular polysaccharides (IPS) in the biofilms.Total amounts of IPS in mg/mg of biofilm dry-weight. The data sh own are mean values (±SD; n = 9) from three independent experiments. Values with an asterisk (*) are significantly different from other group (P<0.05, ANOVA comparison for all pairs using Tukey test); suc+st −0.5% sucrose +1% starch, and suc−1% sucrose.
Mentions: The expression of gene glg (which encodes a glycogen phosphorylase) was enhanced in biofilms formed in the presence of sucrose plus starch at 21 h and 24 h (vs. suc-biofilms; see Data S3) which could reflect in changes on IPS metabolism during the biofilms development process. Indeed, the determination of the IPS content revealed that suc+st-biofilms at 30 h of biofilm growth have significantly higher amounts of IPS compared to biofilms formed in sucrose alone (P<0.05) (Fig.6).

Bottom Line: Overall, the presence of sucrose and starch (suc+st) influenced the dynamics of S. mutans transcriptome (vs. sucrose alone), which may be associated with gradual digestion of starch by surface-adsorbed amylase.In contrast, at 30 h of biofilm development, multiple genes associated with sugar uptake/transport (e.g. maltose), two-component systems, fermentation/glycolysis and iron transport were differentially expressed in suc+st-biofilms (vs. sucrose-biofilms).Our data show complex remodeling of S. mutans-transcriptome in response to changing environmental conditions in situ, which could modulate the dynamics of biofilm development and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Center for Oral Biology and Eastman Department of Dentistry, University of Rochester Medical Center, Rochester, New York, United States of America.

ABSTRACT
The combination of sucrose and starch in the presence of surface-adsorbed salivary α-amylase and bacterial glucosyltransferases increase the formation of a structurally and metabolically distinctive biofilm by Streptococcus mutans. This host-pathogen-diet interaction may modulate the formation of pathogenic biofilms related to dental caries disease. We conducted a comprehensive study to further investigate the influence of the dietary carbohydrates on S. mutans-transcriptome at distinct stages of biofilm development using whole genomic profiling with a new computational tool (MDV) for data mining. S. mutans UA159 biofilms were formed on amylase-active saliva coated hydroxyapatite discs in the presence of various concentrations of sucrose alone (ranging from 0.25 to 5% w/v) or in combination with starch (0.5 to 1% w/v). Overall, the presence of sucrose and starch (suc+st) influenced the dynamics of S. mutans transcriptome (vs. sucrose alone), which may be associated with gradual digestion of starch by surface-adsorbed amylase. At 21 h of biofilm formation, most of the differentially expressed genes were related to sugar metabolism, such as upregulation of genes involved in maltose/maltotriose uptake and glycogen synthesis. In addition, the groEL/groES chaperones were induced in the suc+st-biofilm, indicating that presence of starch hydrolysates may cause environmental stress. In contrast, at 30 h of biofilm development, multiple genes associated with sugar uptake/transport (e.g. maltose), two-component systems, fermentation/glycolysis and iron transport were differentially expressed in suc+st-biofilms (vs. sucrose-biofilms). Interestingly, lytT (bacteria autolysis) was upregulated, which was correlated with presence of extracellular DNA in the matrix of suc+st-biofilms. Specific genes related to carbohydrate uptake and glycogen metabolism were detected in suc+st-biofilms in more than one time point, indicating an association between presence of starch hydrolysates and intracellular polysaccharide storage. Our data show complex remodeling of S. mutans-transcriptome in response to changing environmental conditions in situ, which could modulate the dynamics of biofilm development and pathogenicity.

Show MeSH
Related in: MedlinePlus