Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii

In dental plaque α-haemolytic streptococci, including Streptococcus gordonii, are considered beneficial for oral health. These organisms produce hydrogen peroxide (H₂O₂) at concentrations sufficient to kill many oral bacteria. Streptococci do not produce catalase yet tolerate H₂O₂. We recently demonstrated that coaggregation with Actinomyces naeslundii stabilizes arginine biosynthesis in S. gordonii. Protein arginine residues are sensitive to oxidation by H₂O₂. Here, the ability of A. naeslundii to protect S. gordonii against self-produced H₂O₂ was investigated. Coaggregation with A. naeslundii enabled S. gordonii to grow in the absence of arginine, and promoted survival of S. gordonii following growth with or without added arginine. Arginine-replete S. gordonii monocultures contained 20-30 μM H₂O₂ throughout exponential growth. Actinomyces naeslundii did not produce H ₂O₂ but synthesized catalase, removed H₂O ₂ from coaggregate cultures and decreased protein oxidation in S. gordonii. On solid medium, S. gordonii inhibited growth of A. naeslundii; exogenous catalase overcame this inhibition. In coaggregate cultures, A. naeslundii cell numbers were >90% lower than in monocultures after 24 h. These results indicate that coaggregation with A. naeslundii protects S. gordonii from oxidative damage. However, high cell densities of S. gordonii inhibit A. naeslundii. Therefore, H₂O₂ may drive these organisms towards an ecologically balanced community in natural dental plaque.