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

• Published in: Applied and environmental microbiology Vol. 84; no. 2
• Main Authors: Cheng, Xingqun, Redanz, Sylvio, Cullin, Nyssa, Zhou, Xuedong, Xu, Xin, Joshi, Vrushali, Koley, Dipankar, Merritt, Justin, Kreth, Jens
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 15.01.2018
• Subjects: Acid production; Acids - pharmacology; Bacterial Proteins - metabolism; Biofilms; Dental Caries - microbiology; Dental plaque; Dental Plaque - microbiology; Environmental changes; Environmental conditions; Environmental effects; Gram-positive bacteria; Humans; Hydrogen peroxide; Hydrogen Peroxide - analysis; Hydrogen Peroxide - metabolism; Hydrogen-Ion Concentration; Lactic acid; Metabolism; Mouth - microbiology; pH effects; Physiology; Pyruvic acid; Pyruvic Acid - metabolism; Streptococcus; Streptococcus - drug effects; Streptococcus - metabolism; Streptococcus gordonii - metabolism; Streptococcus infections; Streptococcus mutans - metabolism; Streptococcus sanguis - metabolism; Stress, Physiological - drug effects; microbial ecology; biofilms; Streptococcus
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/AEM.01697-17

Commensal Streptococcus sanguinis and Streptococcus gordonii are pioneer oral biofilm colonizers. Characteristic for both is the SpxB-dependent production of H 2 O 2 , which is crucial for inhibiting competing biofilm members, especially the cariogenic species Streptococcus mutans . H 2 O 2 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 H 2 O 2 production by S. sanguinis and S. gordonii . S. sanguinis H 2 O 2 production was not found to be affected by moderate changes in environmental pH, whereas S. gordonii H 2 O 2 production declined markedly in response to lower pH. Further investigation into the pyruvate node, the central metabolic switch modulating H 2 O 2 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 H 2 O 2 . 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 H 2 O 2 . 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 H 2 O 2 production at a constant level. The differential control of H 2 O 2 production provides important insights into the role of environmental conditions for growth competition of the oral flora.