Hitchhiking, collapse, and contingency in phage infections of migrating bacterial populations

The ISME Journal volume 14, pages2007–2018(2020)Cite this article

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Abstract

Natural bacterial populations are subjected to constant predation pressure by bacteriophages. Bacteria use a variety of molecular mechanisms to defend themselves from phage predation. However, since phages are nonmotile, perhaps the simplest defense against phage is for bacteria to move faster than phages. In particular, chemotaxis, the active migration of bacteria up attractant gradients, may help the bacteria escape slowly diffusing phages. Here we study phage infection dynamics in migrating bacterial populations driven by chemotaxis through low viscosity agar plates. We find that expanding phage–bacteria populations supports two moving fronts, an outermost bacterial front driven by nutrient uptake and chemotaxis and an inner phage front at which the bacterial population collapses due to phage predation. We show that with increasing adsorption rate and initial phage population, the speed of the moving phage front increases, eventually overtaking the bacterial front and driving the system across a transition from a regime where bacterial front speed exceeds that of the phage front to one where bacteria must evolve phage resistance to survive. Our data support the claim that this process requires phage to hitchhike with moving bacteria. A deterministic model recapitulates the transition under the assumption that phage virulence declines with host growth rate which we confirm experimentally. Finally, near the transition between regimes we observe macroscopic fluctuations in bacterial densities at the phage front. Our work opens a new, spatio-temporal, line of investigation into the eco-evolutionary struggle between bacteria and phage.

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Fig. 1: Spatio-temporal dynamics of bacteria and phage in a soft agar plate with 1mM concentration CaCl2.
Fig. 2: Phages or nutrients regulate bacterial abundances depending on initial phage population size and infectivity.
Fig. 3: Bacterial population dynamics with 5 mM CaCl2 and ∼50,000 phage (PFUs) in the inoculum.

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Acknowledgements

This research has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007 2013)/ERC Grant Agreement No. 740704. DP and SK acknowledge the support from the National Science Foundation Physics Frontiers Center Program (PHY 0822613 and PHY 1430124). This work was performed in part at the Aspen Center for Physics, which is supported by National Science Foundation grant PHY 1607611.

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Author notes

  1. These authors contributed equally: Derek Ping, Tong Wang

Affiliations

  1. Department of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana–Champaign, 1110 West Green St., Urbana, IL, 61801, USA

    Derek Ping, Tong Wang, David T. Fraebel, Sergei Maslov & Seppe Kuehn

  2. Center for the Physics of Living Cells, University of Illinois at Urbana–Champaign, 1110 West Green St., Urbana, IL, 61801, USA

    Derek Ping, David T. Fraebel & Seppe Kuehn

  3. Department of Bioengineering and Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana–Champaign, Urbana, IL, 61801, USA

    Sergei Maslov

  4. Center for Models of Life, Niels Bohr Institute, University of Copenhagen, 2100, Copenhagen, Denmark

    Kim Sneppen

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Ping, D., Wang, T., Fraebel, D.T. et al. Hitchhiking, collapse, and contingency in phage infections of migrating bacterial populations. ISME J 14, 2007–2018 (2020). https://doi.org/10.1038/s41396-020-0664-9

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