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    Identification of Virulence-Associated Properties by Comparative Genome Analysis of Streptococcus pneumoniae, S. pseudopneumoniae, S. mitis, Three S. oralis Subspecies, and S. infantis

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    Author
    Kilian, M.
    Tettelin, H.
    Date
    2019
    Journal
    mBio
    Publisher
    American Society for Microbiology
    Type
    Article
    
    Metadata
    Show full item record
    See at
    https://doi.org/10.1128/mBio.01985-19
    https://doi.org/10.1016/j.conctc.2019.100470
    Abstract
    From a common ancestor, Streptococcus pneumoniae and Streptococcus mitis evolved in parallel into one of the most important pathogens and a mutualistic colonizer of humans, respectively. This evolutionary scenario provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. We performed detailed comparisons of 60 genomes of S. pneumoniae, S. mitis, Streptococcus pseudopneumoniae, the three Streptococcus oralis subspecies oralis, tigurinus, and dentisani, and Streptococcus infantis Nonfunctional remnants of ancestral genes in both S. pneumoniae and in S. mitis support the evolutionary model and the concept that evolutionary changes on both sides were required to reach their present relationship to the host. Confirmed by screening of >7,500 genomes, we identified 224 genes associated with virulence. The striking difference to commensal streptococci was the diversity of regulatory mechanisms, including regulation of capsule production, a significantly larger arsenal of enzymes involved in carbohydrate hydrolysis, and proteins known to interfere with innate immune factors. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. In addition to loss of these virulence-associated genes, adaptation of S. mitis to a mutualistic relationship with the host apparently required preservation or acquisition of 25 genes lost or absent from S. pneumoniae Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms. IMPORTANCE: Streptococcus pneumoniae is one of the most important human pathogens but is closely related to Streptococcus mitis, with which humans live in harmony. The fact that the two species evolved from a common ancestor provides a unique basis for studies of both infection-associated properties and properties important for harmonious coexistence with the host. By detailed comparisons of genomes of the two species and other related streptococci, we identified 224 genes associated with virulence and 25 genes unique to the mutualistic species. The exclusive presence of the virulence factors in S. pneumoniae enhances their potential as vaccine components, as a direct impact on beneficial members of the commensal microbiota can be excluded. Successful adaptation of S. mitis and other commensal streptococci to a harmonious relationship with the host relied on genetic stability and properties facilitating life in biofilms. Copyright 2019 Kilian and Tettelin.
    Description
    In initial publication, the wrong file was present for Fig. S3 in the supplemental material. The file was fixed online on 9 September 2019. Erratum at https://doi.org/10.1016/j.conctc.2019.100470
    Keyword
    bacteremia
    commensal
    evolution
    infective endocarditis
    mutualism
    Streptococcus mitis
    Streptococcus oralis
    Streptococcus pneumoniae
    virulence
    Identifier to cite or link to this item
    https://www.scopus.com/inward/record.uri?eid=2-s2.0-85071777651&doi=10.1128%2fmBio.01985-19&partnerID=40&md5=2560b357922f3fbbd95ff465499683c9; http://hdl.handle.net/10713/10828
    ae974a485f413a2113503eed53cd6c53
    10.1128/mBio.01985-19
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