Pyruvate secretion by oral streptococci modulates hydrogen peroxide dependent antagonism

Sylvio Redanz, Puthayalai Treerat, Rong Mu, Ulrike Redanz, Zhengzhong Zou, Dipankar Koley, Justin Merritt, Jens Kreth

Research output: Contribution to journalArticle

Abstract

Many commensal oral streptococci generate H2O2 via pyruvate oxidase (SpxB) to inhibit the growth of competing bacteria like Streptococcus mutans, a major cariogenic species. In Streptococcus sanguinis SK36 (SK36) and Streptococcus gordonii DL1 (DL1), spxB expression and H2O2 release are subject to carbon catabolite repression by the catabolite control protein A (CcpA). Surprisingly, ccpA deletion mutants of SK36 and DL1 fail to inhibit S. mutans despite their production of otherwise inhibitory levels of H2O2. Using H2O2-deficient spxB deletion mutants of SK36 and DL1, it was subsequently discovered that both strains confer protection in trans to other bacteria when H2O2 is added exogenously. This protective effect depends on the direct detoxification of H2O2 by the release of pyruvate. The pyruvate dependent protective effect is also present in other spxB-encoding streptococci, such as the pneumococcus, but is missing from spxB-negative species like S. mutans. Targeted and transposon-based mutagenesis revealed Nox (putative H2O-forming NADH dehydrogenase) as an essential component required for pyruvate release and oxidative protection, while other genes such as sodA and dps play minor roles. Furthermore, pyruvate secretion is only detectable in aerobic growth conditions at biofilm-like cell densities and is responsive to CcpA-dependent catabolite control. This ability of spxB-encoding streptococci reveals a new facet of the competitive interactions between oral commensals and pathobionts and provides a mechanistic basis for the variable levels of inhibitory potential observed among H2O2-producing strains of commensal oral streptococci.

Original languageEnglish (US)
Pages (from-to)1074-1088
Number of pages15
JournalISME Journal
Volume14
Issue number5
DOIs
StatePublished - May 1 2020

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ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Redanz, S., Treerat, P., Mu, R., Redanz, U., Zou, Z., Koley, D., Merritt, J., & Kreth, J. (2020). Pyruvate secretion by oral streptococci modulates hydrogen peroxide dependent antagonism. ISME Journal, 14(5), 1074-1088. https://doi.org/10.1038/s41396-020-0592-8