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Virus-Host Interactions Shape Viral Dispersal Giving Rise to Distinct Classes of Traveling Waves in Spatial Expansions

Michael Hunter, Nikhil Krishnan, Tongfei Liu, Wolfram Möbius, and Diana Fusco
Phys. Rev. X 11, 021066 – Published 29 June 2021
Physics logo See synopsis: Watching a Virus Expand
An article within the collection: Highlights in Experimental Statistical, Biological, and Soft-Matter Physics

Abstract

Reaction-diffusion waves have long been used to describe the growth and spread of populations undergoing a spatial range expansion. Such waves are generally classed as either pulled, where the dynamics are driven by the very tip of the front and stochastic fluctuations are high, or pushed, where cooperation in growth or dispersal results in a bulk-driven wave in which fluctuations are suppressed. These concepts have been well studied experimentally in populations where the cooperation leads to a density-dependent growth rate. By contrast, relatively little is known about experimental populations that exhibit density-dependent dispersal. Using bacteriophage T7 as a test organism, we present novel experimental measurements that demonstrate that the diffusion of phage T7, in a lawn of host E. coli, is hindered by steric interactions with host bacteria cells. The coupling between host density, phage dispersal, and cell lysis caused by viral infection results in an effective density-dependent diffusion coefficient akin to cooperative behavior. Using a system of reaction-diffusion equations, we show that this effect can result in a transition from a pulled to pushed expansion. Moreover, we find that a second, independent density-dependent effect on phage dispersal spontaneously emerges as a result of the viral incubation period, during which, phage is trapped inside the host unable to disperse. Additional stochastic agent-based simulations reveal that lysis time dramatically affects the rate of diversity loss in viral expansions. Taken together, our results indicate both that bacteriophage can be used as a controllable laboratory population to investigate the impact of density-dependent dispersal on evolution, and that the genetic diversity and adaptability of expanding viral populations could be much greater than is currently assumed.

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  • Received 23 October 2020
  • Revised 18 April 2021
  • Accepted 6 May 2021

DOI:https://doi.org/10.1103/PhysRevX.11.021066

Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.

Published by the American Physical Society

Physics Subject Headings (PhySH)

Physics of Living Systems

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This article appears in the following collection:

Highlights in Experimental Statistical, Biological, and Soft-Matter Physics

A collection of recent highlights in experimental Statistical, Biological, and Soft-Matter Physics showcases PRX’s superb quality and topical diversity.

synopsis

Key Image

Watching a Virus Expand

Published 29 June 2021

Bacteria-infecting viruses provide a controllable platform to study the expansion of a virus in a cell population.

See more in Physics

Authors & Affiliations

Michael Hunter1, Nikhil Krishnan1, Tongfei Liu1,2, Wolfram Möbius3,4, and Diana Fusco1,*

  • 1Cavendish Laboratory, University of Cambridge, Cambridge, CB3 0HE, United Kingdom
  • 2Department of Physics, University of Oxford, Oxford, OX1 3PJ, United Kingdom
  • 3Living Systems Institute, University of Exeter, Exeter, EX4 4QD, United Kingdom
  • 4Physics and Astronomy, College of Engineering, Mathematics and Physical Sciences, University of Exeter, Exeter, EX4 4QL, United Kingdom

  • *df390@cam.ac.uk

Popular Summary

The spatial expansion of populations is ubiquitous in nature, from invasive plant species to ancient human communities. These expansions can be classified as one of two types: pulled, where expansion is led by individuals at the perimeter of the population, or pushed, where cooperation among individuals expands the population more from within. Whether a transition from one type of expansion to another can occur in viral populations, whose dynamics is coupled to that of their host, is unknown. Here, we use a model ecosystem of a bacteria-infecting virus, phage T7, and its host, E. coli, to demonstrate that such transitions can occur in viral expansion even if no explicit cooperation among the viral particles exists.

Using numerical models backed up by experiments, we find that an unavoidable feedback between virus and host dynamics triggers a transition from pulled to pushed expansion: Viral dispersal depends on the host density, which is, in turn, dynamically modified by the virus as the expansion advances. We uncover two independent physical mechanisms that contribute to this feedback and determine how host density and the infection parameters that characterize the virus-host interactions affect the transition between different types of expansions.

Our results point to the phage-bacteria system as a highly controllable platform to investigate the dynamics of expanding populations with density-dependent dispersal, with applications both in eco-evolutionary dynamics and in the study of pattern formation. Beyond phages, our findings suggest that viral range expansions might be much more adaptable than previously thought.

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Vol. 11, Iss. 2 — April - June 2021

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