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Phage predation accelerates the spread of plasmid-encoded antibiotic resistance

Author

Listed:
  • Chujin Ruan

    (China Agricultural University
    Swiss Federal Institute of Aquatic Science and Technology (Eawag))

  • Josep Ramoneda

    (Center for Advanced Studies of Blanes (CEAB)
    University of Colorado)

  • Anton Kan

    (Swiss Federal Institute of Technology (ETH))

  • Timothy J. Rudge

    (Newcastle University)

  • Gang Wang

    (China Agricultural University
    China Agricultural University)

  • David R. Johnson

    (Swiss Federal Institute of Aquatic Science and Technology (Eawag)
    University of Bern)

Abstract

Phage predation is generally assumed to reduce microbial proliferation while not contributing to the spread of antibiotic resistance. However, this assumption does not consider the effect of phage predation on the spatial organization of different microbial populations. Here, we show that phage predation can increase the spread of plasmid-encoded antibiotic resistance during surface-associated microbial growth by reshaping spatial organization. Using two strains of the bacterium Escherichia coli, we demonstrate that phage predation slows the spatial segregation of the strains during growth. This increases the number of cell-cell contacts and the extent of conjugation-mediated plasmid transfer between them. The underlying mechanism is that phage predation shifts the location of fastest growth from the biomass periphery to the interior where cells are densely packed and aligned closer to parallel with each other. This creates straighter interfaces between the strains that are less likely to merge together during growth, consequently slowing the spatial segregation of the strains and enhancing plasmid transfer between them. Our results have implications for the design and application of phage therapy and reveal a mechanism for how microbial functions that are deleterious to human and environmental health can proliferate in the absence of positive selection.

Suggested Citation

  • Chujin Ruan & Josep Ramoneda & Anton Kan & Timothy J. Rudge & Gang Wang & David R. Johnson, 2024. "Phage predation accelerates the spread of plasmid-encoded antibiotic resistance," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49840-7
    DOI: 10.1038/s41467-024-49840-7
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    References listed on IDEAS

    as
    1. Yinyin Ma & Josep Ramoneda & David R. Johnson, 2023. "Timing of antibiotic administration determines the spread of plasmid-encoded antibiotic resistance during microbial range expansion," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Bryan T Weinstein & Maxim O Lavrentovich & Wolfram Möbius & Andrew W Murray & David R Nelson, 2017. "Genetic drift and selection in many-allele range expansions," PLOS Computational Biology, Public Library of Science, vol. 13(12), pages 1-31, December.
    3. Tim N. Enke & Gabriel E. Leventhal & Matthew Metzger & José T. Saavedra & Otto X. Cordero, 2018. "Microscale ecology regulates particulate organic matter turnover in model marine microbial communities," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    4. Charlotte Brives & Jessica Pourraz, 2020. "Phage therapy as a potential solution in the fight against AMR: obstacles and possible futures," Palgrave Communications, Palgrave Macmillan, vol. 6(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

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