Genomic and transcriptomic insights into the virulence and adaptation of shock syndrome-causing Streptococcus anginosus

<i>Streptococcus anginosus</i> is a common isolate of the oral cavity and an opportunistic pathogen for systemic infections. Although the pyogenic infections caused by <i>S. anginosus</i> are similar to those caused by <i>Streptococcus pyogenes</i>, <i>S. anginosus</i> lacks most of the well-characterized virulence factors of <i>S. pyogenes</i>. To investigate the pathogenicity of <i>S. anginosus</i>, we analysed the genome of a newly identified <i>S. anginosus</i> strain, KH1, which was associated with toxic shock-like syndrome in an immunocompetent adolescent. The genome of KH1 contains nine genomic islands, two Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/CRISPR-associated systems and many phage-related proteins, indicating that the genome is influenced by prophages and horizontal gene transfer. Comparative genome analysis of 355 <i>S</i>. <i>anginosus</i> strains revealed a significant difference between the sizes of the pan genome and core genome, reflecting notable strain variations. We further analysed the transcriptomes of KH1 under conditions mimicking either the oral cavity or the bloodstream. We found that in an artificial saliva medium, the expression of a putative quorum quenching system and pyruvate oxidase for H₂O₂ production was upregulated, which could optimize the competitiveness of <i>S. anginosus</i> in the oral ecosystem. Conversely, in a modified serum medium, purine and glucan biosynthesis, competence and bacteriocin production were significantly upregulated, likely facilitating the survival of KH1 in the bloodstream. These findings indicate that <i>S. anginosus</i> can utilize diverse mechanisms to adapt to different environmental niches and establish infection, despite its lack of toxin production.