A Multi-Omic View of Host-Pathogen-Commensal Interplay in Salmonella-Mediated Intestinal Infection

Brooke L. Deatherage Kaiser, Jie Li, James A. Sanford, Young Mo Kim, Scott R. Kronewitter, Marcus B. Jones, Christine T. Peterson, Scott N. Peterson, Bryan C. Frank, Samuel O. Purvine, Joseph N. Brown, Thomas O. Metz, Richard D. Smith, Fred Heffron, Joshua N. Adkins

    Research output: Contribution to journalArticle

    50 Scopus citations

    Abstract

    The potential for commensal microorganisms indigenous to a host (the 'microbiome' or 'microbiota') to alter infection outcome by influencing host-pathogen interplay is largely unknown. We used a multi-omics "systems" approach, incorporating proteomics, metabolomics, glycomics, and metagenomics, to explore the molecular interplay between the murine host, the pathogen Salmonella enterica serovar Typhimurium (S. Typhimurium), and commensal gut microorganisms during intestinal infection with S. Typhimurium. We find proteomic evidence that S. Typhimurium thrives within the infected 129/SvJ mouse gut without antibiotic pre-treatment, inducing inflammation and disrupting the intestinal microbiome (e.g., suppressing Bacteroidetes and Firmicutes while promoting growth of Salmonella and Enterococcus). Alteration of the host microbiome population structure was highly correlated with gut environmental changes, including the accumulation of metabolites normally consumed by commensal microbiota. Finally, the less characterized phase of S. Typhimurium's lifecycle was investigated, and both proteomic and glycomic evidence suggests S. Typhimurium may take advantage of increased fucose moieties to metabolize fucose while growing in the gut. The application of multiple omics measurements to Salmonella-induced intestinal inflammation provides insights into complex molecular strategies employed during pathogenesis between host, pathogen, and the microbiome.

    Original languageEnglish (US)
    Article numbere67155
    JournalPloS one
    Volume8
    Issue number6
    DOIs
    StatePublished - Jun 26 2013

    ASJC Scopus subject areas

    • Biochemistry, Genetics and Molecular Biology(all)
    • Agricultural and Biological Sciences(all)
    • General

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  • Cite this

    Deatherage Kaiser, B. L., Li, J., Sanford, J. A., Kim, Y. M., Kronewitter, S. R., Jones, M. B., Peterson, C. T., Peterson, S. N., Frank, B. C., Purvine, S. O., Brown, J. N., Metz, T. O., Smith, R. D., Heffron, F., & Adkins, J. N. (2013). A Multi-Omic View of Host-Pathogen-Commensal Interplay in Salmonella-Mediated Intestinal Infection. PloS one, 8(6), [e67155]. https://doi.org/10.1371/journal.pone.0067155