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Infect while the iron is scarce: nutrient-explicit phage-bacteria games

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Abstract

Marine microbial primary production is influenced by the availability and uptake of essential nutrients, including iron. Although marine microbes have evolved mechanisms to scavenge sub-nanomolar concentrations of iron, recent observations suggest that viruses may co-opt these very same mechanisms to facilitate infection. The “Ferrojan Horse Hypothesis” proposes that viruses incorporate iron atoms into their tail fiber proteins to adsorb to target host receptors. Here, we propose an evolutionary game theoretic approach to consider the joint strategies of hosts and viruses in environments with limited nutrients (like iron). We analyze the bimatrix game and find that evolutionarily stable strategies depend on the stability and quality of nutrient conditions. For example, in highly stable iron conditions, virus pressure does not change host uptake strategies. However, when iron levels are dynamic, virus pressure can lead to fluctuations in the extent to which hosts invest in metabolic machinery that increases both iron uptake and susceptibility to viral infection. Altogether, this evolutionary game model provides further evidence that viral infection and nutrient dynamics jointly shape the fate of microbial populations.

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Data availability

All numerical integrations of ODEs were carried out via the fourth-order Runge–Kutta method as implemented by function ode45 in MATLAB v 2017a. Heteroclinic networks were visualized using R v 3.5.2’s [49] igraph v 1.2.2 [50] package. Scripts are available at https://doi.org/10.5281/zenodo.4750365

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Acknowledgements

The authors would like to thank Stephen Abedon, David Talmy, Mya Breitbart, and Rachel Kuske for their helpful input on manuscript drafts. The authors also thank Stephen J Beckett for code review, and the Simons Collaboration on Ocean Processes and Ecology (SCOPE) community for their support.

Funding

This research was funded by the Simons Foundation (SCOPE Award ID 329018 and 721231).

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Authors and Affiliations

  1. School of Biological Sciences, Georgia Institute of Technology, 950 Atlantic Drive, Atlanta, GA, 30332, USA

    Daniel Muratore & Joshua S. Weitz

  2. School of Physics, Georgia Institute of Technology, 837 State Street, Atlanta, GA, 30332, USA

    Joshua S. Weitz

  3. Interdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, GA, USA

    Daniel Muratore

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  1. Daniel Muratore
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  2. Joshua S. Weitz
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DM and JSW conceived the work, DM performed analysis, and DM and JSW wrote and edited the manuscript.

Corresponding authors

Correspondence to Daniel Muratore or Joshua S. Weitz.

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Muratore, D., Weitz, J.S. Infect while the iron is scarce: nutrient-explicit phage-bacteria games. Theor Ecol 14, 467–487 (2021). https://doi.org/10.1007/s12080-021-00508-8

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  • DOI: https://doi.org/10.1007/s12080-021-00508-8

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