Differential response of Streptococcus mutans towards friend and foe in mixed-species cultures

Abstract

In the oral biofilm, the 'mitis' streptococci are among the first group of organisms to colonize the tooth surface. Their proliferation is thought to be an important factor required for antagonizing the growth of cariogenic species such as Streptococcus mutans. In this study, we used a threespecies mixed culture to demonstrate that another ubiquitous early colonizing species, Veillonella parvula, can greatly affect the outcome of the competition between a pair of antagonists such as S. mutans and Streptococcus gordonii. Transcriptome analysis further revealed that S. mutans responds differentially to its friend (V. parvula) and foe (S. gordonii). In the mixed culture with S. gordonii, all but one of the S. mutans sugar uptake and metabolic genes were downregulated, while genes for alternative energy source utilization and H 2 O 2 tolerance were upregulated, resulting in a slower but persistent growth. In contrast, when cultured with V. parvula, S. mutans grew equally well or better than in monoculture and exhibited relatively few changes within its transcriptome. When V. parvula was introduced into the mixed culture of S. mutans and S. gordonii, it rescued the growth inhibition of S. mutans. In this three-species environment, S. mutans increased the expression of genes required for the uptake and metabolism of minor sugars, while genes required for oxidative stress tolerance were downregulated. We conclude that the major factors that affect the competition between S. mutans and S. gordonii are carbohydrate utilization and H 2 O 2 resistance. The presence of V. parvula in the tri-species culture mitigates these two major factors and allows S. mutans to proliferate, despite the presence of S. gordonii. INTRODUCTIONBiofilms in the human oral cavity are exceptionally diverse and can harbour more than 800 microbial species (Aas et al., 2005;Keijser et al., 2008;Paster et al., 2001Paster et al., , 2006Zaura et al., 2009). Dental biofilm formation is hypothesized to be a sequential process Kolenbrander et al., 2006Kolenbrander et al., , 2010. After a new tooth emerges or a surface is cleaned, the surface is colonized by a group of bacteria named the 'pioneer colonizers', which are composed mostly of the 'mitis' streptococci (i.e. Streptococcus gordonii, Streptococcus sanguinis, Streptococcus mitis, etc.). Subsequently, early colonizers such as Streptococcus mutans and veillonellae, and bridging species such as the fusobacteria, join the community through interactions with the pioneer colonizers or by adhering to the available sites on the tooth surface. Growth of the early colonizers then modifies the local environment, making it favourable for the growth of late colonizers, which consist mostly of Gram-negative, obligate anaerobic bacteria. Eventually, through cell growth and co-adhesion, a mature biofilm is formed (for reviews, see Diaz et al., 2006;Kolenbrander et al., 2010). Once formed, the biofilm composition is relatively stable, featuring high biodiversity; however, environmental perturbation can disrupt this e...

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