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A genome-wide atlas of antibiotic susceptibility targets and pathways to tolerance

Author

Listed:
  • Dmitry Leshchiner

    (Boston College)

  • Federico Rosconi

    (Boston College)

  • Bharathi Sundaresh

    (Boston College)

  • Emily Rudmann

    (Boston College)

  • Luisa Maria Nieto Ramirez

    (Boston College)

  • Andrew T. Nishimoto

    (St. Jude Children’s Research Hospital)

  • Stephen J. Wood

    (Boston College)

  • Bimal Jana

    (Boston College)

  • Noemí Buján

    (Boston College)

  • Kaicheng Li

    (Boston College)

  • Jianmin Gao

    (Boston College)

  • Matthew Frank

    (St. Jude Children’s Research Hospital)

  • Stephanie M. Reeve

    (St. Jude Children’s Research Hospital)

  • Richard E. Lee

    (St. Jude Children’s Research Hospital)

  • Charles O. Rock

    (St. Jude Children’s Research Hospital)

  • Jason W. Rosch

    (St. Jude Children’s Research Hospital)

  • Tim van Opijnen

    (Boston College)

Abstract

Detailed knowledge on how bacteria evade antibiotics and eventually develop resistance could open avenues for novel therapeutics and diagnostics. It is thereby key to develop a comprehensive genome-wide understanding of how bacteria process antibiotic stress, and how modulation of the involved processes affects their ability to overcome said stress. Here we undertake a comprehensive genetic analysis of how the human pathogen Streptococcus pneumoniae responds to 20 antibiotics. We build a genome-wide atlas of drug susceptibility determinants and generated a genetic interaction network that connects cellular processes and genes of unknown function, which we show can be used as therapeutic targets. Pathway analysis reveals a genome-wide atlas of cellular processes that can make a bacterium less susceptible, and often tolerant, in an antibiotic specific manner. Importantly, modulation of these processes confers fitness benefits during active infections under antibiotic selection. Moreover, screening of sequenced clinical isolates demonstrates that mutations in genes that decrease antibiotic sensitivity and increase tolerance readily evolve and are frequently associated with resistant strains, indicating such mutations could be harbingers for the emergence of antibiotic resistance.

Suggested Citation

  • Dmitry Leshchiner & Federico Rosconi & Bharathi Sundaresh & Emily Rudmann & Luisa Maria Nieto Ramirez & Andrew T. Nishimoto & Stephen J. Wood & Bimal Jana & Noemí Buján & Kaicheng Li & Jianmin Gao & M, 2022. "A genome-wide atlas of antibiotic susceptibility targets and pathways to tolerance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30967-4
    DOI: 10.1038/s41467-022-30967-4
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    References listed on IDEAS

    as
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    3. Zeyu Zhu & Defne Surujon & Juan C. Ortiz-Marquez & Wenwen Huo & Ralph R. Isberg & José Bento & Tim van Opijnen, 2020. "Entropy of a bacterial stress response is a generalizable predictor for fitness and antibiotic sensitivity," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    4. Edward Geisinger & Nadav J. Mortman & Yunfei Dai & Murat Cokol & Sapna Syal & Andrew Farinha & Delaney G. Fisher & Amy Y. Tang & David W. Lazinski & Stephen Wood & Jon Anthony & Tim Opijnen & Ralph R., 2020. "Author Correction: Antibiotic susceptibility signatures identify potential antimicrobial targets in the Acinetobacter baumannii cell envelope," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
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