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

Maslov, Sergei; Sneppen, Kim

doi:10.1038/srep10523

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:

Maslov, Sergei ^[1]; Sneppen, Kim ^[2]

Brookhaven National Lab. (BNL), Upton, NY (United States)
Univ. of Copenhagen, Copenhagen (Denmark)

Publication Date:: Tue Jun 02 00:00:00 EDT 2015

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:: 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.

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                    Maslov, Sergei, & Sneppen, Kim. Well-temperate phage: Optimal bet-hedging against local environmental collapses.  United States.  https://doi.org/10.1038/srep10523

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                    Maslov, Sergei, and Sneppen, Kim. Tue .  
"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.

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@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},

  journal      = {Scientific Reports},

  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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The crystal structure of bacteriophage λ RexA provides novel insights into the DNA binding properties of Rex-like phage exclusion proteins

Journal Article Adams, Myfanwy C. ; Schiltz, Carl J. ; Sun, Jing ; ... - Nucleic Acids Research

Abstract RexA and RexB function as an exclusion system that prevents bacteriophage T4rII mutants from growing on Escherichia coli λ phage lysogens. Recent data established that RexA is a non-specific DNA binding protein that can act independently of RexB to bias the λ bistable switch toward the lytic state, preventing conversion back to lysogeny. The molecular interactions underlying these activities are unknown, owing in part to a dearth of structural information. Here, we present the 2.05-Å crystal structure of the λ RexA dimer, which reveals a two-domain architecture with unexpected structural homology to the recombination-associated protein RdgC. Modelling suggests thatmore »« less
https://doi.org/10.1093/nar/gkae212

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

Abstract

Citation Formats

Prokaryotes: The unseen majority journal, June 1998

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 Î¦S1: 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

Responses in continuous cultures of lysogenicEscherichia coli following induction journal, May 1970

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

High abundance of viruses found in aquatic environments journal, August 1989

Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments journal, September 2005

Antagonistic coevolution between a bacterium and a bacteriophage journal, May 2002

Single-cell Analysis of λ Immunity Regulation journal, November 2003

Why Do Phage Play Dice? journal, September 2009

Phage and bacteria support mutual diversity in a narrowing staircase of coexistence journal, May 2014

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

Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand journal, January 1997

A regulatory model for steady-state conditions in populations of lysogenic bacteria journal, January 1968

Correction: Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages journal, August 2006

Antagonistic coevolution between a bacterium and a bacteriophage journal, May 2002

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

Pseudomonas fluorescens infection by bacteriophage Î¦S1: the influence of temperature, host growth phase and media journal, December 2004

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

The population biology of bacterial viruses: Why be temperate journal, August 1984

The Establishment of Lysogenicity in Escherichia coli journal, January 1953

Coexistence of phage and bacteria on the boundary of self-organized refuges journal, July 2012

Ecology and evolution in microbial systems: the generation and maintenance of diversity in phage–host interactions journal, June 2008

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

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

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 journal, February 2016

Estimating Optimal Lysogenic Propensity for Viruses in Stressed Environments preprint, May 2018

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

Prokaryotes: The unseen majority
journal, June 1998

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 Î¦S1: 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

Responses in continuous cultures of lysogenicEscherichia coli following induction
journal, May 1970

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

High abundance of viruses found in aquatic environments
journal, August 1989

Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments
journal, September 2005

Antagonistic coevolution between a bacterium and a bacteriophage
journal, May 2002

Single-cell Analysis of λ Immunity Regulation
journal, November 2003

Why Do Phage Play Dice?
journal, September 2009

Phage and bacteria support mutual diversity in a narrowing staircase of coexistence
journal, May 2014

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

Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand
journal, January 1997

A regulatory model for steady-state conditions in populations of lysogenic bacteria
journal, January 1968

Correction: Viruses' Life History: Towards a Mechanistic Basis of a Trade-Off between Survival and Reproduction among Phages
journal, August 2006

Antagonistic coevolution between a bacterium and a bacteriophage
journal, May 2002

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

Pseudomonas fluorescens infection by bacteriophage Î¦S1: the influence of temperature, host growth phase and media
journal, December 2004

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

The population biology of bacterial viruses: Why be temperate
journal, August 1984

The Establishment of Lysogenicity in Escherichia coli
journal, January 1953

Coexistence of phage and bacteria on the boundary of self-organized refuges
journal, July 2012

Ecology and evolution in microbial systems: the generation and maintenance of diversity in phage–host interactions
journal, June 2008

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

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

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
journal, February 2016

Estimating Optimal Lysogenic Propensity for Viruses in Stressed Environments
preprint, May 2018

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