Plasticity of the Pyruvate Node Modulates Hydrogen Peroxide Production and Acid Tolerance in Multiple Oral Streptococci

Abstract

Commensal Streptococcus sanguinis and Streptococcus gordonii are pioneer oral biofilm colonizers. Characteristic for both is the SpxB-dependent production of H₂O₂, which is crucial for inhibiting competing biofilm members, especially the cariogenic species Streptococcus mutans. H₂O₂ production is strongly affected by environmental conditions, but few mechanisms are known. Dental plaque pH is one of the key parameters dictating dental plaque ecology and ultimately oral health status. Therefore, the objective of the current study was to characterize the effects of environmental pH on H₂O₂ production by S. sanguinis and S. gordonii. S. sanguinis H₂O₂ production was not found to be affected by moderate changes in environmental pH, whereas S. gordonii H₂O₂ production declined markedly in response to lower pH. Further investigation into the pyruvate node, the central metabolic switch modulating H₂O₂ or lactic acid production, revealed increased lactic acid levels for S. gordonii at pH 6. The bias for lactic acid production at pH 6 resulted in concomitant improvement in the survival of S. gordonii at low pH and seems to constitute part of the acid tolerance response of S. gordonii. Differential responses to pH similarly affect other oral streptococcal species, suggesting that the observed results are part of a larger phenomenon linking environmental pH, central metabolism, and the capacity to produce antagonistic amounts of H₂O₂. IMPORTANCE Oral biofilms are subject to frequent and dramatic changes in pH. S. sanguinis and S. gordonii can compete with caries- and periodontitis-associated pathogens by generating H₂O₂. Therefore, it is crucial to understand how S. sanguinis and S. gordonii adapt to low pH and maintain their competitiveness under acid stress. The present study provides evidence that certain oral bacteria respond to environmental pH changes by tuning their metabolic output in favor of lactic acid production, to increase their acid survival, while others maintain their H₂O₂ production at a constant level. The differential control of H₂O₂ production provides important insights into the role of environmental conditions for growth competition of the oral flora.