Abstract

ABSTRACTBacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. Here, we show that dental plaque, saliva, and carious lesions all contain abundant polyphosphate-accumulating bacteria. Saturation state modeling results, informed by phosphate uptake experiments using the model organism Lactobacillus rhamnosus, which is known to inhabit advanced carious lesions, suggest that polyphosphate accumulation can lead to undersaturated conditions with respect to hydroxyapatite under some oral cavity conditions. The cell densities of polyphosphate-accumulating bacteria we observed in some regions of oral biofilms are comparable to those that produce undersaturated conditions (i.e., those that thermodynamically favor mineral dissolution) in our phosphate uptake experiments with L. rhamnosus. These results suggest that the localized generation of undersaturated conditions by polyphosphate-accumulating bacteria constitutes a new potential mechanism of tooth dissolution that may augment the effects of metabolic acid production.IMPORTANCE Dental caries is a serious public health issue that can have negative impacts on overall quality of life and oral health. The role of oral bacteria in the dissolution of dental enamel and dentin that can result in carious lesions has long been solely ascribed to metabolic acid production. Here, we show that certain oral bacteria may act as a dynamic shunt for phosphate in dental biofilms via the accumulation of a polymer known as polyphosphate—potentially mediating phosphate-dependent conditions such as caries (dental decay).

Highlights

  • Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater

  • While previous researchers proposed that the synthesis of polyphosphate by Streptococcus may play a role in caries [17,18,19], the influence of diverse polyphosphate-accumulating bacteria on mineral saturation state has not, to our knowledge, been applied to the oral environment, where we show that biofilms in plaque and saliva contain abundant polyphosphate-accumulating bacteria that may chemically exchange ions with the calcium phosphate minerals that comprise the inorganic portion of the tooth

  • To address several different facets of the hypothesis that polyP-accumulating bacteria (PAB) may affect localized chemical saturation in the oral cavity, we analyzed genomic databases of oral taxa, we quantified PAB in clinical samples of plaque, saliva, and dentinal lesions, we conducted phosphate uptake experiments using a defined in vitro single-species model, and we modeled the potential impact of polyP accumulation on the saturation state of saliva

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Summary

Introduction

Bacteria that accumulate polyphosphates have previously been shown to dynamically influence the solubility of phosphatic minerals in marine settings and wastewater. We provide evidence in support of the novel hypothesis that certain oral bacteria may play a considerable role in dynamically modulating the ion concentrations of PO43Ϫ, and the saturation state/solubility of calcium phosphate minerals at the tooth/plaque interface, through intracellular polyphosphate (polyP) accumulation. While previous researchers proposed that the synthesis of polyphosphate by Streptococcus may play a role in caries [17,18,19], the influence of diverse polyphosphate-accumulating bacteria on mineral saturation state has not, to our knowledge, been applied to the oral environment, where we show that biofilms in plaque and saliva contain abundant polyphosphate-accumulating bacteria that may chemically exchange ions with the calcium phosphate minerals that comprise the inorganic portion of the tooth.

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