Journal Article

Dynamics of Streptococcus mutans Transcriptome in Response to Starch and Sucrose during Biofilm Development

Lin, Amy H.-M., Lee, Herbert, Lemos, José A., Koo, Hyun, Agidi, Senyo, Klein, Marlise I., Hamaker, Bruce R., Xie, Gary, DeBaz, Lena

2010

Overview

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.

• Publisher: Public Library of Science,Public Library of Science (PLoS)
• Subject: Acids / Amylases / Autolysis / Bacteria / bacterial biofilms / Base Sequence / BASIC BIOLOGICAL SCIENCES / Biofilms / Biology / Carbohydrate metabolism / Carbohydrates / Chaperones / Computer applications / Data mining / Data processing / Dental caries / Dentistry / Deoxyribonucleic acid / Developmental stages / Diet / DNA / DNA Primers / DNA-binding proteins / Environmental changes / Environmental conditions / Environmental stress / Enzymes / Fermentation / Fluorides / Food science / Gene expression / Gene Expression Profiling / Genes / Genes, Bacterial / Genetics and Genomics/Bioinformatics / Genetics and Genomics/Gene Expression / Glucose metabolism / Glycogen / Glycolysis / Hydrolysates / Hydroxyapatite / Hydroxyapatites / Immunology / Infectious Diseases/Bacterial Infections / Iron / Iron transport / Laboratories / Maltose / Maltotriose / Metabolism / microarrays / Microbiology/Applied Microbiology / Microbiology/Environmental Microbiology / Microbiology/Medical Microbiology / Oligonucleotide Array Sequence Analysis / Pathogenesis / Pathogenicity / Pathogens / Potassium / Reverse Transcriptase Polymerase Chain Reaction / Saliva / Sediments / Software / Starch / Starch - pharmacology / starches / Streptococcus infections / Streptococcus mutans / Streptococcus mutans - drug effects / Streptococcus mutans - genetics / Studies / Sucrose / Sucrose - pharmacology / Sugar / Transport / α-Amylase