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

Derek Ping, Tong Wang, David T. Fraebel, Sergei Maslov, Kim Sneppen, View ORCID ProfileSeppe Kuehn
doi: https://doi.org/10.1101/378596
Derek Ping
aDepartment of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
dCenter for the Physics of Living Cells, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
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Tong Wang
aDepartment of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
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David T. Fraebel
aDepartment of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
dCenter for the Physics of Living Cells, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
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Sergei Maslov
bDepartment of Bioengineering and Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA
aDepartment of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
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  • For correspondence: seppe.kuehn@gmail.com ksneppen@gmail.com ssmaslov@gmail.com
Kim Sneppen
cCenter for Models of Life, Niels Bohr Institute, University of Copenhagen, 2100 Copenhagen, Denmark
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  • For correspondence: seppe.kuehn@gmail.com ksneppen@gmail.com ssmaslov@gmail.com
Seppe Kuehn
aDepartment of Physics, Loomis Laboratory of Physics, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
dCenter for the Physics of Living Cells, University of Illinois at Urbana-Champaign, 1110 West Green St., Urbana, IL 61801, USA
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  • ORCID record for Seppe Kuehn
  • For correspondence: seppe.kuehn@gmail.com ksneppen@gmail.com ssmaslov@gmail.com
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Abstract

Natural bacterial populations are subject to constant predation pressure by phages. Bacteria use a variety of well-studied molecular mechanisms to defend themselves from phage predation. However, since phage are non-motile, perhaps the simplest defense against phage would be for bacteria to outrun their predators. 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 support two migrating fronts, an outermost “bacterial” front driven by nutrient uptake and chemotaxis and an inner “phage” front at which bacterial population collapses due to phage predation. We show that with increasing adsorption rate and initial phage population, the rate of migration of the phage front increases, eventually overtaking the bacterial front and driving the system across a “phage transition” from a regime where bacteria outrun a phage infection to one where they must evolve phage resistance to survive. We confirm experimentally that this process requires phages to “surf” the bacterial front by repeatedly reinfecting the fastest moving bacteria. A deterministic model recapitulates the transition. Macroscopic fluctuations in bacterial densities at the phage front suggest that a feedback mechanism, possibly due to growth rate dependent phage infection rates, drives millimeter scale spatial structure in phage-bacteria populations. Our work opens a new, spatiotemporal, line of investigation into the eco-evolutionary struggle between bacteria and their phage predators.

Significance Statement The infection of bacteria by phage requires physical contact. This fact means that motile bacteria may avoid non-motile phage by simply running away. By this mechanism bacterial chemotaxis may help bacteria to escape phages. Here we show that when phage infect bacteria moving in soft agar plates, high phage populations or infectivity rates result in phages stopping and killing all bacteria. Conversely, when initial phage numbers or infectivity rates are low, bacteria are able to migrate away from phage successfully, despite phage ability to “surf” bacterial fronts for more than 24 hours. Between these regimes we document a “phage transition” where bacterial physiology and contingency in phage infection manifest through large-scale fluctuations in spatio-temporal dynamics.

Footnotes

  • D.P. performed the experiments. T.W. developed and simulated models, analyzed data, made figures. D.T.F. assisted D.P. with experiments. K.S., S.M. and S.K. designed experiments, analyzed data, made figures, wrote the paper.

  • Authors declare no conflicts of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 28, 2018.
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Hitchhiking, collapse and contingency in phage infections of migrating bacterial populations
Derek Ping, Tong Wang, David T. Fraebel, Sergei Maslov, Kim Sneppen, Seppe Kuehn
bioRxiv 378596; doi: https://doi.org/10.1101/378596
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Hitchhiking, collapse and contingency in phage infections of migrating bacterial populations
Derek Ping, Tong Wang, David T. Fraebel, Sergei Maslov, Kim Sneppen, Seppe Kuehn
bioRxiv 378596; doi: https://doi.org/10.1101/378596

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