A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection

Paolo Marcatili, Martin W. Nielsen, Thomas Sicheritz-Ponten, Tim K. Jensen, Claus Schafer-Nielsen, Mette Boye, Morten Nielsen, Kirstine Klitgaard

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    Abstract

    Background: Polymicrobial infections represent a great challenge for the clarification of disease etiology and the
    development of comprehensive diagnostic or therapeutic tools, particularly for fastidious and difficult-to-cultivate
    bacteria. Using bovine digital dermatitis (DD) as a disease model, we introduce a novel strategy to study the
    pathogenesis of complex infections.
    Results: The strategy combines meta-transcriptomics with high-density peptide-microarray technology to screen
    for in vivo-expressed microbial genes and the host antibody response at the site of infection. Bacterial expression
    patterns supported the assumption that treponemes were the major DD pathogens but also indicated the active
    involvement of other phyla (primarily Bacteroidetes). Bacterial genes involved in chemotaxis, flagellar synthesis and
    protection against oxidative and acidic stress were among the major factors defining the disease.
    Conclusions: The extraordinary diversity observed in bacterial expression, antigens and host antibody responses
    between individual cows pointed toward microbial variability as a hallmark of DD. Persistence of infection and DD
    reinfection in the same individual is common; thus, high microbial diversity may undermine the host’s capacity to
    mount an efficient immune response and maintain immunological memory towards DD. The common antigenic
    markers identified here using a high-density peptide microarray address this issue and may be useful for future
    preventive measures against DD.
    Original languageEnglish
    Article number987
    JournalBMC Genomics
    Volume17
    Number of pages14
    ISSN1471-2164
    DOIs
    Publication statusPublished - 5. Dec 2016

    Cite this

    Marcatili, P., Nielsen, M. W., Sicheritz-Ponten, T., Jensen, T. K., Schafer-Nielsen, C., Boye, M., ... Klitgaard, K. (2016). A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection. BMC Genomics, 17, [987]. https://doi.org/10.1186/s12864-016-3341-7
    Marcatili, Paolo ; Nielsen, Martin W. ; Sicheritz-Ponten, Thomas ; Jensen, Tim K. ; Schafer-Nielsen, Claus ; Boye, Mette ; Nielsen, Morten ; Klitgaard, Kirstine . / A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection. In: BMC Genomics. 2016 ; Vol. 17.
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    abstract = "Background: Polymicrobial infections represent a great challenge for the clarification of disease etiology and thedevelopment of comprehensive diagnostic or therapeutic tools, particularly for fastidious and difficult-to-cultivatebacteria. Using bovine digital dermatitis (DD) as a disease model, we introduce a novel strategy to study thepathogenesis of complex infections.Results: The strategy combines meta-transcriptomics with high-density peptide-microarray technology to screenfor in vivo-expressed microbial genes and the host antibody response at the site of infection. Bacterial expressionpatterns supported the assumption that treponemes were the major DD pathogens but also indicated the activeinvolvement of other phyla (primarily Bacteroidetes). Bacterial genes involved in chemotaxis, flagellar synthesis andprotection against oxidative and acidic stress were among the major factors defining the disease.Conclusions: The extraordinary diversity observed in bacterial expression, antigens and host antibody responsesbetween individual cows pointed toward microbial variability as a hallmark of DD. Persistence of infection and DDreinfection in the same individual is common; thus, high microbial diversity may undermine the host’s capacity tomount an efficient immune response and maintain immunological memory towards DD. The common antigenicmarkers identified here using a high-density peptide microarray address this issue and may be useful for futurepreventive measures against DD.",
    keywords = "Integrated pipeline, RNAseq, Digital dermatitis, High-density peptide arrays",
    author = "Paolo Marcatili and Nielsen, {Martin W.} and Thomas Sicheritz-Ponten and Jensen, {Tim K.} and Claus Schafer-Nielsen and Mette Boye and Morten Nielsen and Kirstine Klitgaard",
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    Marcatili, P, Nielsen, MW, Sicheritz-Ponten, T, Jensen, TK, Schafer-Nielsen, C, Boye, M, Nielsen, M & Klitgaard, K 2016, 'A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection', BMC Genomics, vol. 17, 987. https://doi.org/10.1186/s12864-016-3341-7

    A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection. / Marcatili, Paolo ; Nielsen, Martin W.; Sicheritz-Ponten, Thomas; Jensen, Tim K.; Schafer-Nielsen, Claus; Boye, Mette; Nielsen, Morten; Klitgaard, Kirstine .

    In: BMC Genomics, Vol. 17, 987, 05.12.2016.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - A novel approach to probe host-pathogen interactions of bovine digital dermatitis, a model of a complex polymicrobial infection

    AU - Marcatili, Paolo

    AU - Nielsen, Martin W.

    AU - Sicheritz-Ponten, Thomas

    AU - Jensen, Tim K.

    AU - Schafer-Nielsen, Claus

    AU - Boye, Mette

    AU - Nielsen, Morten

    AU - Klitgaard, Kirstine

    PY - 2016/12/5

    Y1 - 2016/12/5

    N2 - Background: Polymicrobial infections represent a great challenge for the clarification of disease etiology and thedevelopment of comprehensive diagnostic or therapeutic tools, particularly for fastidious and difficult-to-cultivatebacteria. Using bovine digital dermatitis (DD) as a disease model, we introduce a novel strategy to study thepathogenesis of complex infections.Results: The strategy combines meta-transcriptomics with high-density peptide-microarray technology to screenfor in vivo-expressed microbial genes and the host antibody response at the site of infection. Bacterial expressionpatterns supported the assumption that treponemes were the major DD pathogens but also indicated the activeinvolvement of other phyla (primarily Bacteroidetes). Bacterial genes involved in chemotaxis, flagellar synthesis andprotection against oxidative and acidic stress were among the major factors defining the disease.Conclusions: The extraordinary diversity observed in bacterial expression, antigens and host antibody responsesbetween individual cows pointed toward microbial variability as a hallmark of DD. Persistence of infection and DDreinfection in the same individual is common; thus, high microbial diversity may undermine the host’s capacity tomount an efficient immune response and maintain immunological memory towards DD. The common antigenicmarkers identified here using a high-density peptide microarray address this issue and may be useful for futurepreventive measures against DD.

    AB - Background: Polymicrobial infections represent a great challenge for the clarification of disease etiology and thedevelopment of comprehensive diagnostic or therapeutic tools, particularly for fastidious and difficult-to-cultivatebacteria. Using bovine digital dermatitis (DD) as a disease model, we introduce a novel strategy to study thepathogenesis of complex infections.Results: The strategy combines meta-transcriptomics with high-density peptide-microarray technology to screenfor in vivo-expressed microbial genes and the host antibody response at the site of infection. Bacterial expressionpatterns supported the assumption that treponemes were the major DD pathogens but also indicated the activeinvolvement of other phyla (primarily Bacteroidetes). Bacterial genes involved in chemotaxis, flagellar synthesis andprotection against oxidative and acidic stress were among the major factors defining the disease.Conclusions: The extraordinary diversity observed in bacterial expression, antigens and host antibody responsesbetween individual cows pointed toward microbial variability as a hallmark of DD. Persistence of infection and DDreinfection in the same individual is common; thus, high microbial diversity may undermine the host’s capacity tomount an efficient immune response and maintain immunological memory towards DD. The common antigenicmarkers identified here using a high-density peptide microarray address this issue and may be useful for futurepreventive measures against DD.

    KW - Integrated pipeline, RNAseq, Digital dermatitis, High-density peptide arrays

    U2 - 10.1186/s12864-016-3341-7

    DO - 10.1186/s12864-016-3341-7

    M3 - Journal article

    VL - 17

    JO - B M C Genomics

    JF - B M C Genomics

    SN - 1471-2164

    M1 - 987

    ER -