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

Title: The mobility of packaged phage genome controls ejection dynamics

Abstract

The cell decision between lytic and lysogenic infection is strongly influenced by dynamics of DNA injection into a cell from a phage population, as phages compete for limited resources and progeny. However, what controls the timing of viral DNA ejection events was not understood. This in vitro study reveals that DNA ejection dynamics for phages can be synchronized (occurring within seconds) or desynchronized (displaying minutes-long delays in initiation) based on mobility of encapsidated DNA, which in turn is regulated by environmental factors, such as temperature and extra-cellular ionic conditions. This mechano-regulation of ejection dynamics is suggested to influence viral replication where the cell’s decision between lytic and latent infection is associated with synchronized or desynchronized delayed ejection events from phage population adsorbed to a cell. Our findings are of significant importance for understanding regulatory mechanisms of latency in phage and Herpesviruses, where encapsidated DNA undergoes a similar mechanical transition.

Authors:
ORCiD logo [1]
  1. Department of Pathobiology, Division of Microbiology and Immunology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Champaign, United States; Department of Experimental Medical Sciences, Virus Biophysics Group, Lund University, Lund, Sweden
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
NSFOTHER
OSTI Identifier:
1478089
Resource Type:
Journal Article
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 7; Journal Issue: 2018; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
ENGLISH

Citation Formats

Evilevitch, Alex. The mobility of packaged phage genome controls ejection dynamics. United States: N. p., 2018. Web. doi:10.7554/eLife.37345.
Evilevitch, Alex. The mobility of packaged phage genome controls ejection dynamics. United States. doi:10.7554/eLife.37345.
Evilevitch, Alex. Tue . "The mobility of packaged phage genome controls ejection dynamics". United States. doi:10.7554/eLife.37345.
@article{osti_1478089,
title = {The mobility of packaged phage genome controls ejection dynamics},
author = {Evilevitch, Alex},
abstractNote = {The cell decision between lytic and lysogenic infection is strongly influenced by dynamics of DNA injection into a cell from a phage population, as phages compete for limited resources and progeny. However, what controls the timing of viral DNA ejection events was not understood. This in vitro study reveals that DNA ejection dynamics for phages can be synchronized (occurring within seconds) or desynchronized (displaying minutes-long delays in initiation) based on mobility of encapsidated DNA, which in turn is regulated by environmental factors, such as temperature and extra-cellular ionic conditions. This mechano-regulation of ejection dynamics is suggested to influence viral replication where the cell’s decision between lytic and latent infection is associated with synchronized or desynchronized delayed ejection events from phage population adsorbed to a cell. Our findings are of significant importance for understanding regulatory mechanisms of latency in phage and Herpesviruses, where encapsidated DNA undergoes a similar mechanical transition.},
doi = {10.7554/eLife.37345},
journal = {eLife},
issn = {2050-084X},
number = 2018,
volume = 7,
place = {United States},
year = {2018},
month = {9}
}

Works referenced in this record:

A Single-Molecule Hershey-Chase Experiment
journal, July 2012


Polyamines: Mysterious Modulators of Cellular Functions
journal, May 2000

  • Igarashi, Kazuei; Kashiwagi, Keiko
  • Biochemical and Biophysical Research Communications, Vol. 271, Issue 3
  • DOI: 10.1006/bbrc.2000.2601

Mechanics of DNA packaging in viruses
journal, March 2003

  • Purohit, P. K.; Kondev, J.; Phillips, R.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 6
  • DOI: 10.1073/pnas.0737893100

Lysogenization by bacteriophage lambda: I. Multiple infection and the lysogenic response
journal, January 1973

  • Kourilsky, Philippe
  • MGG Molecular & General Genetics, Vol. 122, Issue 2
  • DOI: 10.1007/BF00435190

Can Changes in Temperature or Ionic Conditions Modify the DNA Organization in the Full Bacteriophage Capsid?
journal, April 2016

  • Frutos, Marta de; Leforestier, Amélie; Degrouard, Jéril
  • The Journal of Physical Chemistry B, Vol. 120, Issue 26
  • DOI: 10.1021/acs.jpcb.6b01783

Salt-Dependent DNA-DNA Spacings in Intact Bacteriophage λ Reflect Relative Importance of DNA Self-Repulsion and Bending Energies
journal, January 2011


Osmotic pressure inhibition of DNA ejection from phage
journal, July 2003

  • Evilevitch, A.; Lavelle, L.; Knobler, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 16
  • DOI: 10.1073/pnas.1233721100

Building a Virus from Scratch: Assembly of an Infectious Virus Using Purified Components in a Rigorously Defined Biochemical Assay System
journal, April 2006

  • Gaussier, Hélène; Yang, Qin; Catalano, Carlos Enrique
  • Journal of Molecular Biology, Vol. 357, Issue 4
  • DOI: 10.1016/j.jmb.2006.01.013

The evolution of life history trade-offs in viruses
journal, October 2014


On Kinetics of Phage Adsorption
journal, July 2007


Decision Making at a Subcellular Level Determines the Outcome of Bacteriophage Infection
journal, May 2010


A Kinetic Analysis of DNA Ejection from Tailed Phages Revealing the Prerequisite Activation Energy
journal, December 2007


Real-time observations of single bacteriophage   DNA ejections in vitro
journal, September 2007

  • Grayson, P.; Han, L.; Winther, T.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 37
  • DOI: 10.1073/pnas.0703274104

Variability of HIV infections
journal, March 1992


Fate-Regulating Circuits in Viruses: From Discovery to New Therapy Targets
journal, September 2017


Events in lambda injection between phage adsorption and DNA entry
journal, July 1976


Lysogenization by bacteriophage lambda
journal, February 1975


Late-Arriving Signals Contribute Less to Cell-Fate Decisions
journal, November 2017


kinITC: A New Method for Obtaining Joint Thermodynamic and Kinetic Data by Isothermal Titration Calorimetry
journal, December 2011

  • Burnouf, Dominique; Ennifar, Eric; Guedich, Sondes
  • Journal of the American Chemical Society, Vol. 134, Issue 1
  • DOI: 10.1021/ja209057d

HIV-1 Dynamics in Vivo: Virion Clearance Rate, Infected Cell Life-Span, and Viral Generation Time
journal, March 1996


Solid-to-fluid-like DNA transition in viruses facilitates infection
journal, September 2014

  • Liu, T.; Sae-Ueng, U.; Li, D.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 41
  • DOI: 10.1073/pnas.1321637111

CRISPR–Cas systems exploit viral DNA injection to establish and maintain adaptive immunity
journal, March 2017

  • Modell, Joshua W.; Jiang, Wenyan; Marraffini, Luciano A.
  • Nature, Vol. 544, Issue 7648
  • DOI: 10.1038/nature21719

Ionic switch controls the DNA state in phage λ
journal, June 2015

  • Li, Dong; Liu, Ting; Zuo, Xiaobing
  • Nucleic Acids Research, Vol. 43, Issue 13
  • DOI: 10.1093/nar/gkv611

DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry
journal, February 2010

  • Jeembaeva, Meerim; Jönsson, Bengt; Castelnovo, Martin
  • Journal of Molecular Biology, Vol. 395, Issue 5
  • DOI: 10.1016/j.jmb.2009.11.069

The Growth of Bacteriophage
journal, January 1939


Characterization of exponentially modified Gaussian peaks in chromatography
journal, September 1972


Forces and Pressures in DNA Packaging and Release from Viral Capsids
journal, March 2003


Evolvability of an RNA virus is determined by its mutational neighbourhood
journal, August 2000

  • Burch, Christina L.; Chao, Lin
  • Nature, Vol. 406, Issue 6796
  • DOI: 10.1038/35020564

Amplification and Spread of Viruses in a Growing Plaque
journal, October 1999


Internal DNA pressure modifies stability of WT phage
journal, May 2007

  • Ivanovska, I.; Wuite, G.; Jonsson, B.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 23
  • DOI: 10.1073/pnas.0703166104

Single DNA molecule jamming and history-dependent dynamics during motor-driven viral packaging
journal, May 2016

  • Keller, Nicholas; Grimes, Shelley; Jardine, Paul J.
  • Nature Physics, Vol. 12, Issue 8
  • DOI: 10.1038/nphys3740

DNA ejection from bacteriophage: Towards a general behavior for osmotic-suppression experiments
journal, August 2007


Antiserum inhibition of propagating viruses
journal, August 1997


Challenging Packaging Limits and Infectivity of Phage λ
journal, January 2012

  • Nurmemmedov, Elmar; Castelnovo, Martin; Medina, Elizabeth
  • Journal of Molecular Biology, Vol. 415, Issue 2
  • DOI: 10.1016/j.jmb.2011.11.015

Herpes Virus Genome, The Pressure Is On
journal, July 2013

  • Bauer, David W.; Huffman, Jamie B.; Homa, Fred L.
  • Journal of the American Chemical Society, Vol. 135, Issue 30
  • DOI: 10.1021/ja404008r

DNA arrangement in isometric phage heads
journal, August 1977

  • Earnshaw, W. C.; Harrison, S. C.
  • Nature, Vol. 268, Issue 5621
  • DOI: 10.1038/268598a0

Bacteriophage lambda: Early pioneer and still relevant
journal, May 2015


Recombination Promoted by DNA Viruses: Phage λ to Herpes Simplex Virus
journal, September 2014


DNA bending-induced phase transition of encapsidated genome in phage  
journal, February 2013

  • Lander, G. C.; Johnson, J. E.; Rau, D. C.
  • Nucleic Acids Research, Vol. 41, Issue 8
  • DOI: 10.1093/nar/gkt137

Solid-to-fluid DNA transition inside HSV-1 capsid close to the temperature of infection
journal, September 2014

  • Sae-Ueng, Udom; Li, Dong; Zuo, Xiaobing
  • Nature Chemical Biology, Vol. 10, Issue 10
  • DOI: 10.1038/nchembio.1628

Effects of Salt Concentrations and Bending Energy on the Extent of Ejection of Phage Genomes
journal, February 2008


Conditions for the Infection of Escherichia coli with Lambda Phage and for the Establishment of Lysogeny
journal, December 1959


Bacteriophage evolution given spatial constraint
journal, September 2007


Influence of Internal DNA Pressure on Stability and Infectivity of Phage λ
journal, October 2015


Portal Stability Controls Dynamics of DNA Ejection from Phage
journal, April 2016

  • Freeman, Krista G.; Behrens, Manja A.; Streletzky, Kiril A.
  • The Journal of Physical Chemistry B, Vol. 120, Issue 26
  • DOI: 10.1021/acs.jpcb.6b04172

Compartmentalization of Spermine and Spermidine in the Herpes Simplex Virion
journal, November 1971

  • Gibson, W.; Roizman, B.
  • Proceedings of the National Academy of Sciences, Vol. 68, Issue 11
  • DOI: 10.1073/pnas.68.11.2818

Putrescine and certain polyamines can inhibit DNA injection from bacteriophage lambda
journal, August 1975


Exploring the Balance between DNA Pressure and Capsid Stability in Herpesviruses and Phages
journal, July 2015

  • Bauer, D. W.; Li, D.; Huffman, J.
  • Journal of Virology, Vol. 89, Issue 18
  • DOI: 10.1128/JVI.01172-15

Multiplexing Genetic and Nucleosome Positioning Codes: A Computational Approach
journal, June 2016


Effects of bacteriophage traits on plaque formation
journal, January 2011


Cell fate decisions emerge as phages cooperate or compete inside their host
journal, February 2017

  • Trinh, Jimmy T.; Székely, Tamás; Shao, Qiuyan
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14341

Nonequilibrium dynamics and ultraslow relaxation of confined DNA during viral packaging
journal, May 2014

  • Berndsen, Z. T.; Keller, N.; Grimes, S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 23
  • DOI: 10.1073/pnas.1405109111

Stochastic gene expression as a molecular switch for viral latency
journal, August 2009


DNA Ejection from an Archaeal Virus—A Single-Molecule Approach
journal, May 2013


Dynamics of Double Stranded DNA Reptation From Bacteriophage
journal, April 1992


Determination of cell fate selection during phage lambda infection
journal, December 2008

  • St-Pierre, F.; Endy, D.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 52
  • DOI: 10.1073/pnas.0808831105

Dynamic and static light scattering analysis of DNA ejection from the phage λ
journal, July 2007


Curve Fitting for Restoration of Accuracy for Overlapping Peaks in Gas Chromatography/Combustion Isotope Ratio Mass Spectrometry
journal, April 1994

  • Goodman, Keith J.; Brenna, J. Thomas.
  • Analytical Chemistry, Vol. 66, Issue 8
  • DOI: 10.1021/ac00080a015