Phage predation accelerates the spread of plasmid-encoded antibiotic resistance

Chujin Ruan, Josep Ramoneda, Anton Kan, Timothy J. Rudge, Gang Wang () and David R. Johnson ()
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Chujin Ruan: China Agricultural University
Josep Ramoneda: Center for Advanced Studies of Blanes (CEAB)
Anton Kan: Swiss Federal Institute of Technology (ETH)
Timothy J. Rudge: Newcastle University
Gang Wang: China Agricultural University
David R. Johnson: Swiss Federal Institute of Aquatic Science and Technology (Eawag)

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-49840-7

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