Abstract
Streptococcus mutans is considered the principal cariogenic bacterium for dental caries. Despite the recognition of their importance for cariogenesis, the possible coordination among S. mutans’ main virulence factors, including glucan production, acidogenicity and aciduricity, has been less well studied. In the present study, using S. mutans strains with surface-displayed pH-sensitive pHluorin, we revealed sucrose availability- and Gtf functionality-dependent proton accumulation on S. mutans surface. Consistent with this, using a pH-sensitive dye, we demonstrated that both in vivo cell-produced and in vitro enzymatically synthesized insoluble glucans displayed proton-concentrating ability. Global transcriptomics revealed proton accumulation triggers the up-regulation of genes encoding functions involved in acid tolerance response in a glucan-dependent manner. Our data suggested that this proton enrichment around S. mutans could pre-condition the bacterium for acid-stress. Consistent with this hypothesis, we found S. mutans strains defective in glucan production were more acid sensitive. Our study revealed for the first time that insoluble glucans is likely an essential factor linking acidogenicity with aciduricity. The coordination of these key virulence factors could provide new insights on how S. mutans may have become a major cariogenic pathogen.
Highlights
Dental caries is one of the most prevalent bacteria-related infectious diseases worldwide[1,2]
The observation that a well-maintained, lower pH was monitored on the cell surface than in the macro-environment suggested the potential involvement of S. mutans surface-associated component, likely insoluble glucans in concentrating protons on cell surface
Results showed that when S. mutans wildtype or gtfBC mutant pre-grown in the buffered MDM supplemented with sucrose was submerged in pH 5.5 buffer containing pHrodo Green dye, cells displayed bright fluorescence signal (Fig. 2A)
Summary
Sucrose availability- and Gtf functionality-dependent proton accumulation on S. mutans cell surface. In contrast to parent strain O87, GtfBC-defective strain grown in the presence or absence of sucrose exhibited a significantly less change (p < 0.05) in fluorescence intensity when switched from pH 7.5 buffer to each tested buffer with lower pH value (Fig. 1) These data showed that the pH reduction on the cell surface is associated with S. mutans’ GtfBC activity and dependent on the availability of sucrose. Compared to wild-type, the gtfBC mutant defective in synthesizing insoluble glucans suffered significantly more viability loss (p < 0.05) when exposed to the lethal pH (with survival rate of 12.67% and 0.0005% after 0.5 h and 1 h exposure, respectively) even after being pre-grown in the presence of sucrose (Fig. 4). The results further demonstrate the important role of insoluble glucans in linking S. mutans’ acidogenicity and aciduricity
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