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Roving methyltransferases generate a mosaic epigenetic landscape and influence evolution in Bacteroides fragilis group

Author

Listed:
  • Michael J. Tisza

    (LCIM, NIAID, NIH
    Baylor College of Medicine)

  • Derek D. N. Smith

    (LCIM, NIAID, NIH
    Wildlife Toxicology Research Section)

  • Andrew E. Clark

    (NIH
    University of Texas Southwestern Medical Center)

  • Jung-Ho Youn

    (NIH)

  • Pavel P. Khil

    (LCIM, NIAID, NIH
    NIH)

  • John P. Dekker

    (LCIM, NIAID, NIH
    NIH)

Abstract

Three types of DNA methyl modifications have been detected in bacterial genomes, and mechanistic studies have demonstrated roles for DNA methylation in physiological functions ranging from phage defense to transcriptional control of virulence and host-pathogen interactions. Despite the ubiquity of methyltransferases and the immense variety of possible methylation patterns, epigenomic diversity remains unexplored for most bacterial species. Members of the Bacteroides fragilis group (BFG) reside in the human gastrointestinal tract as key players in symbiotic communities but also can establish anaerobic infections that are increasingly multi-drug resistant. In this work, we utilize long-read sequencing technologies to perform pangenomic (n = 383) and panepigenomic (n = 268) analysis of clinical BFG isolates cultured from infections seen at the NIH Clinical Center over four decades. Our analysis reveals that single BFG species harbor hundreds of DNA methylation motifs, with most individual motif combinations occurring uniquely in single isolates, implying immense unsampled methylation diversity within BFG epigenomes. Mining of BFG genomes identified more than 6000 methyltransferase genes, approximately 1000 of which were associated with intact prophages. Network analysis revealed substantial gene flow among disparate phage genomes, implying a role for genetic exchange between BFG phages as one of the ultimate sources driving BFG epigenome diversity.

Suggested Citation

  • Michael J. Tisza & Derek D. N. Smith & Andrew E. Clark & Jung-Ho Youn & Pavel P. Khil & John P. Dekker, 2023. "Roving methyltransferases generate a mosaic epigenetic landscape and influence evolution in Bacteroides fragilis group," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39892-6
    DOI: 10.1038/s41467-023-39892-6
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    References listed on IDEAS

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    1. Daniel H Huson & Sina Beier & Isabell Flade & Anna Górska & Mohamed El-Hadidi & Suparna Mitra & Hans-Joachim Ruscheweyh & Rewati Tappu, 2016. "MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-12, June.
    2. Guillaume Gautreau & Adelme Bazin & Mathieu Gachet & Rémi Planel & Laura Burlot & Mathieu Dubois & Amandine Perrin & Claudine Médigue & Alexandra Calteau & Stéphane Cruveiller & Catherine Matias & Chr, 2020. "PPanGGOLiN: Depicting microbial diversity via a partitioned pangenome graph," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-27, March.
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