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Title: Well-temperate phage: Optimal bet-hedging against local environmental collapses

Abstract

Upon infection of their bacterial hosts temperate phages must chose between lysogenic and lytic developmental strategies. Here we apply the game-theoretic bet-hedging strategy introduced by Kelly to derive the optimal lysogenic fraction of the total population of phages as a function of frequency and intensity of environmental downturns affecting the lytic subpopulation. “Well-temperate” phage from our title is characterized by the best long-term population growth rate. We show that it is realized when the lysogenization frequency is approximately equal to the probability of lytic population collapse. We further predict the existence of sharp boundaries in system’s environmental, ecological, and biophysical parameters separating the regions where this temperate strategy is optimal from those dominated by purely virulent or dormant (purely lysogenic) strategies. We show that the virulent strategy works best for phages with large diversity of hosts, and access to multiple independent environments reachable by diffusion. Conversely, progressively more temperate or even dormant strategies are favored in the environments, that are subject to frequent and severe temporal downturns.

Authors:
 [1];  [2]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States)
  2. Univ. of Copenhagen, Copenhagen (Denmark)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1213376
Report Number(s):
BNL-108254-2015-JA
Journal ID: ISSN 2045-2322; R&D Project: PM-031; KP1601040
Grant/Contract Number:  
SC00112704
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 5; Journal Issue: 8; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; computational models; information theory and computation

Citation Formats

Maslov, Sergei, and Sneppen, Kim. Well-temperate phage: Optimal bet-hedging against local environmental collapses. United States: N. p., 2015. Web. doi:10.1038/srep10523.
Maslov, Sergei, & Sneppen, Kim. Well-temperate phage: Optimal bet-hedging against local environmental collapses. United States. https://doi.org/10.1038/srep10523
Maslov, Sergei, and Sneppen, Kim. 2015. "Well-temperate phage: Optimal bet-hedging against local environmental collapses". United States. https://doi.org/10.1038/srep10523. https://www.osti.gov/servlets/purl/1213376.
@article{osti_1213376,
title = {Well-temperate phage: Optimal bet-hedging against local environmental collapses},
author = {Maslov, Sergei and Sneppen, Kim},
abstractNote = {Upon infection of their bacterial hosts temperate phages must chose between lysogenic and lytic developmental strategies. Here we apply the game-theoretic bet-hedging strategy introduced by Kelly to derive the optimal lysogenic fraction of the total population of phages as a function of frequency and intensity of environmental downturns affecting the lytic subpopulation. “Well-temperate” phage from our title is characterized by the best long-term population growth rate. We show that it is realized when the lysogenization frequency is approximately equal to the probability of lytic population collapse. We further predict the existence of sharp boundaries in system’s environmental, ecological, and biophysical parameters separating the regions where this temperate strategy is optimal from those dominated by purely virulent or dormant (purely lysogenic) strategies. We show that the virulent strategy works best for phages with large diversity of hosts, and access to multiple independent environments reachable by diffusion. Conversely, progressively more temperate or even dormant strategies are favored in the environments, that are subject to frequent and severe temporal downturns.},
doi = {10.1038/srep10523},
url = {https://www.osti.gov/biblio/1213376}, journal = {Scientific Reports},
issn = {2045-2322},
number = 8,
volume = 5,
place = {United States},
year = {Tue Jun 02 00:00:00 EDT 2015},
month = {Tue Jun 02 00:00:00 EDT 2015}
}

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Cited by: 43 works
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Works referencing / citing this record:

When to be temperate: on the fitness benefits of lysis vs. lysogeny
journal, May 2020


Inevitability of Genetic Parasites
journal, August 2016


A Growing Microcolony can Survive and Support Persistent Propagation of Virulent Phages
posted_content, June 2017


Viral invasion fitness across a continuum from lysis to latency†
journal, January 2019


In silico Evolution of Lysis-Lysogeny Strategies Reproduces Observed Lysogeny Propensities in Temperate Bacteriophages
journal, July 2017


Models of life: epigenetics, diversity and cycles
journal, March 2017


When to wake up? The optimal waking-up strategies for starvation-induced persistence
posted_content, November 2020


Inevitability of Genetic Parasites
journal, August 2016


Diversity waves in collapse-driven population dynamics
journal, July 2015


Pseudo-chaotic oscillations in CRISPR-virus coevolution predicted by bifurcation analysis
journal, July 2014


Carriage of λ Latent Virus Is Costly for Its Bacterial Host due to Frequent Reactivation in Monoxenic Mouse Intestine
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When to wake up? The optimal waking-up strategies for starvation-induced persistence
journal, February 2021


Population Dynamics of Phage and Bacteria in Spatially Structured Habitats Using Phage λ and Escherichia coli
journal, April 2016


Viruses and mobile elements as drivers of evolutionary transitions
journal, August 2016


A growing microcolony can survive and support persistent propagation of virulent phages
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Commentary: A Host-Produced Quorum-Sensing Autoinducer Controls a Phage Lysis-Lysogeny Decision
journal, June 2019


Optimized bacteria are environmental prediction engines
journal, July 2018


How pirate phage interferes with helper phage: Comparison of the two distinct strategies
posted_content, November 2019


When to be temperate: on the fitness benefits of lysis vs. lysogeny
journal, May 2020


A growing microcolony can survive and support persistent propagation of virulent phages
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When to be Temperate: On the Fitness Benefits of Lysis vs. Lysogeny
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Long-term persistence of agricultural pest insects by risk-spreading dispersal
journal, May 2018


Commentary: A Host-Produced Quorum-Sensing Autoinducer Controls a Phage Lysis-Lysogeny Decision
journal, June 2019