A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis

M. Lappann, H. Claus, T. van Alen, Morten Harmsen, J. Elias, Søren Molin, U. Vogel

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    P>Major pathogenic clonal complexes (cc) of Neisseria meningitidis differ substantially in their point prevalence among healthy carriers. We show that frequently carried pathogenic cc (e.g. sequence type ST-41/44 cc and ST-32 cc) depend on extracellular DNA (eDNA) to initiate in vitro biofilm formation, whereas biofilm formation of cc with low point prevalence (ST-8 cc and ST-11 cc) was eDNA-independent. For initial biofilm formation, a ST-32 cc type strain, but not a ST-11 type strain, utilized eDNA. The release of eDNA was mediated by lytic transglycosylase and cytoplasmic N-acetylmuramyl-l-alanine amidase genes. In late biofilms, outer membrane phospholipase A-dependent autolysis, which was observed in most cc, but not in ST-8 and ST-11 strains, was required for shear force resistance of microcolonies. Taken together, N. meningitidis evolved two different biofilm formation strategies, an eDNA-dependent one yielding shear force resistant microcolonies, and an eDNA-independent one. Based on the experimental findings and previous epidemiological observations, we hypothesize that most meningococcal cc display a settler phenotype, which is eDNA-dependent and results in a stable interaction with the host. On the contrary, spreaders (ST-11 and ST-8 cc) are unable to use eDNA for biofilm formation and might compensate for poor colonization properties by high transmission rates.
    Original languageEnglish
    JournalMolecular Microbiology
    Volume75
    Issue number6
    Pages (from-to)1355-1371
    ISSN0950-382X
    DOIs
    Publication statusPublished - 2010

    Cite this

    Lappann, M. ; Claus, H. ; van Alen, T. ; Harmsen, Morten ; Elias, J. ; Molin, Søren ; Vogel, U. / A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. In: Molecular Microbiology. 2010 ; Vol. 75, No. 6. pp. 1355-1371.
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    title = "A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis",
    abstract = "P>Major pathogenic clonal complexes (cc) of Neisseria meningitidis differ substantially in their point prevalence among healthy carriers. We show that frequently carried pathogenic cc (e.g. sequence type ST-41/44 cc and ST-32 cc) depend on extracellular DNA (eDNA) to initiate in vitro biofilm formation, whereas biofilm formation of cc with low point prevalence (ST-8 cc and ST-11 cc) was eDNA-independent. For initial biofilm formation, a ST-32 cc type strain, but not a ST-11 type strain, utilized eDNA. The release of eDNA was mediated by lytic transglycosylase and cytoplasmic N-acetylmuramyl-l-alanine amidase genes. In late biofilms, outer membrane phospholipase A-dependent autolysis, which was observed in most cc, but not in ST-8 and ST-11 strains, was required for shear force resistance of microcolonies. Taken together, N. meningitidis evolved two different biofilm formation strategies, an eDNA-dependent one yielding shear force resistant microcolonies, and an eDNA-independent one. Based on the experimental findings and previous epidemiological observations, we hypothesize that most meningococcal cc display a settler phenotype, which is eDNA-dependent and results in a stable interaction with the host. On the contrary, spreaders (ST-11 and ST-8 cc) are unable to use eDNA for biofilm formation and might compensate for poor colonization properties by high transmission rates.",
    author = "M. Lappann and H. Claus and {van Alen}, T. and Morten Harmsen and J. Elias and S{\o}ren Molin and U. Vogel",
    year = "2010",
    doi = "10.1111/j.1365-2958.2010.07054.x",
    language = "English",
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    pages = "1355--1371",
    journal = "Molecular Microbiology",
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    Lappann, M, Claus, H, van Alen, T, Harmsen, M, Elias, J, Molin, S & Vogel, U 2010, 'A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis', Molecular Microbiology, vol. 75, no. 6, pp. 1355-1371. https://doi.org/10.1111/j.1365-2958.2010.07054.x

    A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. / Lappann, M.; Claus, H.; van Alen, T.; Harmsen, Morten; Elias, J.; Molin, Søren; Vogel, U.

    In: Molecular Microbiology, Vol. 75, No. 6, 2010, p. 1355-1371.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis

    AU - Lappann, M.

    AU - Claus, H.

    AU - van Alen, T.

    AU - Harmsen, Morten

    AU - Elias, J.

    AU - Molin, Søren

    AU - Vogel, U.

    PY - 2010

    Y1 - 2010

    N2 - P>Major pathogenic clonal complexes (cc) of Neisseria meningitidis differ substantially in their point prevalence among healthy carriers. We show that frequently carried pathogenic cc (e.g. sequence type ST-41/44 cc and ST-32 cc) depend on extracellular DNA (eDNA) to initiate in vitro biofilm formation, whereas biofilm formation of cc with low point prevalence (ST-8 cc and ST-11 cc) was eDNA-independent. For initial biofilm formation, a ST-32 cc type strain, but not a ST-11 type strain, utilized eDNA. The release of eDNA was mediated by lytic transglycosylase and cytoplasmic N-acetylmuramyl-l-alanine amidase genes. In late biofilms, outer membrane phospholipase A-dependent autolysis, which was observed in most cc, but not in ST-8 and ST-11 strains, was required for shear force resistance of microcolonies. Taken together, N. meningitidis evolved two different biofilm formation strategies, an eDNA-dependent one yielding shear force resistant microcolonies, and an eDNA-independent one. Based on the experimental findings and previous epidemiological observations, we hypothesize that most meningococcal cc display a settler phenotype, which is eDNA-dependent and results in a stable interaction with the host. On the contrary, spreaders (ST-11 and ST-8 cc) are unable to use eDNA for biofilm formation and might compensate for poor colonization properties by high transmission rates.

    AB - P>Major pathogenic clonal complexes (cc) of Neisseria meningitidis differ substantially in their point prevalence among healthy carriers. We show that frequently carried pathogenic cc (e.g. sequence type ST-41/44 cc and ST-32 cc) depend on extracellular DNA (eDNA) to initiate in vitro biofilm formation, whereas biofilm formation of cc with low point prevalence (ST-8 cc and ST-11 cc) was eDNA-independent. For initial biofilm formation, a ST-32 cc type strain, but not a ST-11 type strain, utilized eDNA. The release of eDNA was mediated by lytic transglycosylase and cytoplasmic N-acetylmuramyl-l-alanine amidase genes. In late biofilms, outer membrane phospholipase A-dependent autolysis, which was observed in most cc, but not in ST-8 and ST-11 strains, was required for shear force resistance of microcolonies. Taken together, N. meningitidis evolved two different biofilm formation strategies, an eDNA-dependent one yielding shear force resistant microcolonies, and an eDNA-independent one. Based on the experimental findings and previous epidemiological observations, we hypothesize that most meningococcal cc display a settler phenotype, which is eDNA-dependent and results in a stable interaction with the host. On the contrary, spreaders (ST-11 and ST-8 cc) are unable to use eDNA for biofilm formation and might compensate for poor colonization properties by high transmission rates.

    U2 - 10.1111/j.1365-2958.2010.07054.x

    DO - 10.1111/j.1365-2958.2010.07054.x

    M3 - Journal article

    VL - 75

    SP - 1355

    EP - 1371

    JO - Molecular Microbiology

    JF - Molecular Microbiology

    SN - 0950-382X

    IS - 6

    ER -