skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Scientific Reports
DOI:https://doi.org/10.1038/srep10523· OSTI ID:1213376
 [1];  [2]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States)
  2. Univ. of Copenhagen, Copenhagen (Denmark)

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.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC00112704
OSTI ID:
1213376
Report Number(s):
BNL-108254-2015-JA; R&D Project: PM-031; KP1601040
Journal Information:
Scientific Reports, Vol. 5, Issue 8; ISSN 2045-2322
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 43 works
Citation information provided by
Web of Science

References (39)

Prokaryotes: The unseen majority journal June 1998
Optimizing reproduction in a randomly varying environment journal September 1966
Explaining microbial population genomics through phage predation journal November 2009
Conditions for the Existence of Bacteriophage journal June 1961
Optimal Investment Strategy for Risky Assets journal July 1998
The Growth of Bacteriophage journal January 1939
Pseudomonas fluorescens infection by bacteriophage ΦS1: the influence of temperature, host growth phase and media journal December 2004
Phage and bacteria support mutual diversity in a narrowing staircase of coexistence journal May 2014
Single-cell Analysis of λ Immunity Regulation journal November 2003
Shannon information and biological fitness conference January 2004
Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments journal September 2005
High abundance of viruses found in aquatic environments journal August 1989
Responses in continuous cultures of lysogenicEscherichia coli following induction journal May 1970
Establishment of Repression by Lambdoid Phage in Catabolite Activator Protein and Adenylate Cyclase Mutants of Escherichia coli journal February 1972
The Establishment of Lysogenicity in Escherichia coli journal January 1953
Alternative stable states in host–phage dynamics journal June 2007
How should we define ‘fitness’ for general ecological scenarios? journal June 1992
The population biology of bacterial viruses: Why be temperate journal August 1984
Reticulate Representation of Evolutionary and Functional Relationships between Phage Genomes journal February 2008
A New Interpretation of Information Rate journal July 1956
Delayed germination of seeds: Cohen's model revisited journal December 1984
Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages journal June 2006
Antagonistic coevolution between a bacterium and a bacteriophage journal May 2002
Why Do Phage Play Dice? journal September 2009
Fixed points and limit cycles in the population dynamics of lysogenic viruses and their hosts journal July 2010
Ecology and evolution in microbial systems: the generation and maintenance of diversity in phage–host interactions journal June 2008
A regulatory model for steady-state conditions in populations of lysogenic bacteria journal January 1968
Proteolytic cleavage of bacteriophage lambda repressor in induction. journal January 1975
Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand journal January 1997
Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors journal July 2002
Correction: Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages journal August 2006
Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems. journal January 1985
Dynamical optimization theory of a diversified portfolio journal May 1998
The bacteriophages journal February 1969
Resource-Limited Growth, Competition, and Predation: A Model and Experimental Studies with Bacteria and Bacteriophage journal January 1977
Lysogenization by bacteriophage lambda: I. Multiple infection and the lysogenic response journal January 1973
Coevolutionary arms races between bacteria and bacteriophage journal June 2005
Bacterial Persistence: A Model of Survival in Changing Environments journal January 2005
Coexistence of phage and bacteria on the boundary of self-organized refuges journal July 2012

Cited By (28)

How pirate phage interferes with helper phage: Comparison of the two distinct strategies journal February 2020
The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition journal March 2019
How repeated outbreaks drive the evolution of bacteriophage communication: Insights from a mathematical model posted_content April 2020
The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition journal December 2019
When to be temperate: on the fitness benefits of lysis vs. lysogeny journal May 2020
Prediction and Power in Molecular Sensors: Uncertainty and Dissipation When Conditionally Markovian Channels Are Driven by Semi-Markov Environments preprint January 2017
Characterization of the vaginal DNA virome in health and dysbiosis: an opening study in patients with non-female factor infertility preprint September 2019
Inevitability of Genetic Parasites journal August 2016
When to wake up? The optimal waking-up strategies for starvation-induced persistence preprint January 2019
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
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 journal February 2016
Estimating Optimal Lysogenic Propensity for Viruses in Stressed Environments preprint May 2018
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 journal December 2017
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 posted_content February 2020
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