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Antibiotic collateral sensitivity is contingent on the repeatability of evolution

Author

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  • Daniel Nichol

    (University of Oxford
    H. Lee Moffitt Cancer Center and Research Institute
    The Institute of Cancer Research)

  • Joseph Rutter

    (Louis Stokes Department of Veterans Affairs Hospital)

  • Christopher Bryant

    (Case Western Reserve University School of Medicine)

  • Andrea M. Hujer

    (Louis Stokes Department of Veterans Affairs Hospital
    Case Western Reserve University School of Medicine)

  • Sai Lek

    (The Jackson Laboratory for Genomic Medicine)

  • Mark D. Adams

    (The Jackson Laboratory for Genomic Medicine)

  • Peter Jeavons

    (University of Oxford)

  • Alexander R. A. Anderson

    (H. Lee Moffitt Cancer Center and Research Institute)

  • Robert A. Bonomo

    (Louis Stokes Department of Veterans Affairs Hospital
    Case Western Reserve University School of Medicine
    Case Western Reserve University School of Medicine
    Case Western Reserve University School of Medicine)

  • Jacob G. Scott

    (Case Western Reserve University School of Medicine
    University of Oxford
    Cleveland Clinic)

Abstract

Antibiotic resistance represents a growing health crisis that necessitates the immediate discovery of novel treatment strategies. One such strategy is the identification of collateral sensitivities, wherein evolution under a first drug induces susceptibility to a second. Here, we report that sequential drug regimens derived from in vitro evolution experiments may have overstated therapeutic benefit, predicting a collaterally sensitive response where cross-resistance ultimately occurs. We quantify the likelihood of this phenomenon by use of a mathematical model parametrised with combinatorially complete fitness landscapes for Escherichia coli. Through experimental evolution we then verify that a second drug can indeed stochastically exhibit either increased susceptibility or increased resistance when following a first. Genetic divergence is confirmed as the driver of this differential response through targeted and whole genome sequencing. Taken together, these results highlight that the success of evolutionarily-informed therapies is predicated on a rigorous probabilistic understanding of the contingencies that arise during the evolution of drug resistance.

Suggested Citation

  • Daniel Nichol & Joseph Rutter & Christopher Bryant & Andrea M. Hujer & Sai Lek & Mark D. Adams & Peter Jeavons & Alexander R. A. Anderson & Robert A. Bonomo & Jacob G. Scott, 2019. "Antibiotic collateral sensitivity is contingent on the repeatability of evolution," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-018-08098-6
    DOI: 10.1038/s41467-018-08098-6
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    Cited by:

    1. Jeff Maltas & Kevin B Wood, 2019. "Pervasive and diverse collateral sensitivity profiles inform optimal strategies to limit antibiotic resistance," PLOS Biology, Public Library of Science, vol. 17(10), pages 1-34, October.
    2. Dennis Y. Liu & Laura Phillips & Darryl M. Wilson & Kelly M. Fulton & Susan M. Twine & Alex Wong & Roger G. Linington, 2023. "Collateral sensitivity profiling in drug-resistant Escherichia coli identifies natural products suppressing cephalosporin resistance," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Natalie J. E. Waller & Chen-Yi Cheung & Gregory M. Cook & Matthew B. McNeil, 2023. "The evolution of antibiotic resistance is associated with collateral drug phenotypes in Mycobacterium tuberculosis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Sara Hernando-Amado & Pablo Laborda & José Luis Martínez, 2023. "Tackling antibiotic resistance by inducing transient and robust collateral sensitivity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. Qian Li & Shang Chen & Kui Zhu & Xiaoluo Huang & Yucheng Huang & Zhangqi Shen & Shuangyang Ding & Danxia Gu & Qiwen Yang & Hongli Sun & Fupin Hu & Hui Wang & Jiachang Cai & Bing Ma & Rong Zhang & Jian, 2022. "Collateral sensitivity to pleuromutilins in vancomycin-resistant Enterococcus faecium," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. Cheng Zhao & Yu Wang & Ranya Mulchandani & Thomas P. Van Boeckel, 2024. "Global surveillance of antimicrobial resistance in food animals using priority drugs maps," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

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