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Hydrolyzed Ce(IV) salts limit sucrose-dependent biofilm formation by Streptococcus mutans.

ABSTRACT: Several studies have focused on the antimicrobial effects of cerium oxide nanoparticles (CeO2-NP) but few have focused on their effects on bacteria under initial biofilm formation conditions. Streptococcus mutans is a prolific biofilm former contributing to dental caries in the presence of fermentable carbohydrates and is a recognized target for therapeutic intervention. CeO2-NP derived solely from Ce(IV) salt hydrolysis were found to reduce adherent bacteria by approximately 40% while commercial dispersions of "bare" CeO2-NP (e.g., 3 nm, 10-20 nm, 30 nm diameter) and Ce(NO3)3·6H2O were either inactive or observed to slightly increase biofilm formation under similar in vitro conditions. Planktonic growth and dispersal assays support a non-bactericidal mode of biofilm inhibition active in the initial phases of S. mutans biofilm production. Human cell proliferation assays suggest only minor effects of hydrolyzed Ce(IV) salts on cellular metabolism at concentrations up to 1 mM Ce, with less observed toxicity compared to equimolar concentrations of AgNO3. The results presented herein have implications in clinical dentistry.

SUBMITTER: Bhatt L

PROVIDER: S-EPMC7233464 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Hydrolyzed Ce(IV) salts limit sucrose-dependent biofilm formation by Streptococcus mutans.

Bhatt Lopa L Chen Lin L Guo Jinglong J Klie Robert F RF Shi Junhe J Pesavento Russell P RP

Journal of inorganic biochemistry 20200111

Several studies have focused on the antimicrobial effects of cerium oxide nanoparticles (CeO<sub>2</sub>-NP) but few have focused on their effects on bacteria under initial biofilm formation conditions. Streptococcus mutans is a prolific biofilm former contributing to dental caries in the presence of fermentable carbohydrates and is a recognized target for therapeutic intervention. CeO<sub>2</sub>-NP derived solely from Ce(IV) salt hydrolysis were found to reduce adherent bacteria by approximate ...[more]

PMID: 32169780

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Project description:Streptococcus mutans is the primary etiological agent of dental caries and causes tooth decay by forming a firmly attached biofilm on tooth surfaces. Biofilm formation is induced by the presence of sucrose, which is a substrate for the synthesis of extracellular polysaccharides but not in the presence of oligosaccharides. Nonetheless, in this study, we found that raffinose, which is an oligosaccharide with an intestinal regulatory function and antiallergic effect, induced biofilm formation by S. mutans in a mixed culture with sucrose, which was at concentrations less than those required to induce biofilm formation directly. We analyzed the possible mechanism behind the small requirement for sucrose for biofilm formation in the presence of raffinose. Our results suggested that sucrose contributed to an increase in bacterial cell surface hydrophobicity and biofilm formation. Next, we examined how the effects of raffinose interacted with the effects of sucrose for biofilm formation. We showed that the presence of raffinose induced fructan synthesis by fructosyltransferase and aggregated extracellular DNA (eDNA, which is probably genomic DNA released from dead cells) into the biofilm. eDNA seemed to be important for biofilm formation, because the degradation of DNA by DNase I resulted in a significant reduction in biofilm formation. When assessing the role of fructan in biofilm formation, we found that fructan enhanced eDNA-dependent cell aggregation. Therefore, our results show that raffinose and sucrose have cooperative effects and that this induction of biofilm formation depends on supportive elements that mainly consist of eDNA and fructan.IMPORTANCE The sucrose-dependent mechanism of biofilm formation in Streptococcus mutans has been studied extensively. Nonetheless, the effects of carbohydrates other than sucrose are inadequately understood. Our findings concerning raffinose advance the understanding of the mechanism underlying the joint effects of sucrose and other carbohydrates on biofilm formation. Since raffinose has been reported to have positive effects on enterobacterial flora, research on the effects of raffinose on the oral flora are required prior to its use as a beneficial sugar for human health. Here, we showed that raffinose induced biofilm formation by S. mutans in low concentrations of sucrose. The induction of biofilm formation generally generates negative effects on the oral flora. Therefore, we believe that this finding will aid in the development of more effective oral care techniques to maintain oral flora health.

Project description:The combination of sucrose and starch in the presence of surface-adsorbed salivary ?-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.

Dataset Information

Hydrolyzed Ce(IV) salts limit sucrose-dependent biofilm formation by Streptococcus mutans.

Publications

Hydrolyzed Ce(IV) salts limit sucrose-dependent biofilm formation by Streptococcus mutans.

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