Ionic switch controls the DNA state in phage λ

Li, Dong; Liu, Ting; Zuo, Xiaobing; Li, Tao; Qiu, Xiangyun; Evilevitch, Alex

doi:10.1093/nar/gkv611

Title: Ionic switch controls the DNA state in phage λ

Abstract

We have recently found that DNA packaged in phage λ undergoes a disordering transition triggered by temperature, which results in increased genome mobility. This solid-to-fluid like DNA transition markedly increases the number of infectious λ particles facilitating infection. However, the structural transition strongly depends on temperature and ionic conditions in the surrounding medium. Using titration microcalorimetry combined with solution X-ray scattering, we mapped both energetic and structural changes associated with transition of the encapsidated λ-DNA. Packaged DNA needs to reach a critical stress level in order for transition to occur. We varied the stress on DNA in the capsid by changing the temperature, packaged DNA length and ionic conditions. We found striking evidence that the intracapsid DNA transition is ‘switched on’ at the ionic conditions mimicking those in vivo and also at the physiologic temperature of infection at 37°C. This ion regulated on-off switch of packaged DNA mobility in turn affects viral replication. The results suggest a remarkable adaptation of phage λ to the environment of its host bacteria in the human gut. The metastable DNA state in the capsid provides a new paradigm for the physical evolution of viruses.

Authors:

Li, Dong ^[1]; Liu, Ting ^[1]; Zuo, Xiaobing ^[2]; Li, Tao ^[2]; Qiu, Xiangyun ^[3]; Evilevitch, Alex ^[4]

Carnegie Mellon Univ., Pittsburgh, PA (United States). Physics Dept.
Argonne National Lab., Argonne, IL (United States). Advanced Photon Source, X-ray Science Div.
George Washington Univ., Washington, DC (United States). Dept. of Physics.
Carnegie Mellon Univ., Pittsburgh, PA (United States). Physics Dept.; Lund Univ., Lund (Sweden). Dept. of Biochemistry and Structural Biology.

Publication Date:: Fri Jun 19 00:00:00 EDT 2015

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1221840

Grant/Contract Number:: AC02-06CH11357

Resource Type:: Accepted Manuscript

Journal Name:: Nucleic Acids Research

Additional Journal Information:: Journal Volume: 43; Journal Issue: 13; Journal ID: ISSN 0305-1048

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Li, Dong, Liu, Ting, Zuo, Xiaobing, Li, Tao, Qiu, Xiangyun, and Evilevitch, Alex. Ionic switch controls the DNA state in phage λ.  United States: N. p., 2015. 
Web.  doi:10.1093/nar/gkv611.

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                    Li, Dong, Liu, Ting, Zuo, Xiaobing, Li, Tao, Qiu, Xiangyun, & Evilevitch, Alex. Ionic switch controls the DNA state in phage λ.  United States.  https://doi.org/10.1093/nar/gkv611

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                    Li, Dong, Liu, Ting, Zuo, Xiaobing, Li, Tao, Qiu, Xiangyun, and Evilevitch, Alex. Fri .  
"Ionic switch controls the DNA state in phage λ".  United States.  https://doi.org/10.1093/nar/gkv611.  https://www.osti.gov/servlets/purl/1221840.

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@article{osti_1221840,

  title        = {Ionic switch controls the DNA state in phage λ},

  author       = {Li, Dong and Liu, Ting and Zuo, Xiaobing and Li, Tao and Qiu, Xiangyun and Evilevitch, Alex},

  abstractNote = {We have recently found that DNA packaged in phage λ undergoes a disordering transition triggered by temperature, which results in increased genome mobility. This solid-to-fluid like DNA transition markedly increases the number of infectious λ particles facilitating infection. However, the structural transition strongly depends on temperature and ionic conditions in the surrounding medium. Using titration microcalorimetry combined with solution X-ray scattering, we mapped both energetic and structural changes associated with transition of the encapsidated λ-DNA. Packaged DNA needs to reach a critical stress level in order for transition to occur. We varied the stress on DNA in the capsid by changing the temperature, packaged DNA length and ionic conditions. We found striking evidence that the intracapsid DNA transition is ‘switched on’ at the ionic conditions mimicking those in vivo and also at the physiologic temperature of infection at 37°C. This ion regulated on-off switch of packaged DNA mobility in turn affects viral replication. The results suggest a remarkable adaptation of phage λ to the environment of its host bacteria in the human gut. The metastable DNA state in the capsid provides a new paradigm for the physical evolution of viruses.},

  doi          = {10.1093/nar/gkv611},

  journal      = {Nucleic Acids Research},

  number       = 13,

  volume       = 43,

  place        = {United States},

  year         = {Fri Jun 19 00:00:00 EDT 2015},

  month        = {Fri Jun 19 00:00:00 EDT 2015}

}

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Liu, T.; Sae-Ueng, U.; Li, D.
Proceedings of the National Academy of Sciences, Vol. 111, Issue 41
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DNA packaging and ejection forces in bacteriophage
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Kindt, J.; Tzlil, S.; Ben-Shaul, A.
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Du, Quan; Kotlyar, Alexander; Vologodskii, Alexander
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Effect of Salt Shock on Stability of λimm434 Lysogens
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Shkilnyj, Paul; Koudelka, Gerald B.
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Defect in the Formation of 70S Ribosomes Caused by Lack of Ribosomal Protein L34 Can Be Suppressed by Magnesium
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Akanuma, Genki; Kobayashi, Ako; Suzuki, Shota
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Metal ion content of Escherichia coli versus cell age.
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Elliott, Gillian; O’Hare, Peter
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Sequestered end products and enzyme regulation: the case of ornithine decarboxylase
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Davis, R. H.; Morris, D. R.; Coffino, P.
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Hydration Forces
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Effects of Salt Concentrations and Bending Energy on the Extent of Ejection of Phage Genomes
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Evilevitch, Alex; Fang, Li Tai; Yoffe, Aron M.
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Works referencing / citing this record:

The mobility of packaged phage genome controls ejection dynamics
journal, September 2018

Evilevitch, Alex
eLife, Vol. 7
DOI: 10.7554/elife.37345

The effects of a knot and its conformational relaxation on the ejection of a single polymer chain from confinement
journal, August 2019

Park, Chung Bin; Kwon, Seulki; Sung, Bong June
The Journal of Chemical Physics, Vol. 151, Issue 5
DOI: 10.1063/1.5110428

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Solid-to-fluid – like DNA transition in viruses facilitates infection

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Releasing the packaged viral DNA into the host cell is an essential process to initiate viral infection. In many double-stranded DNA bacterial viruses and herpesviruses, the tightly packaged genome is hexagonally ordered and stressed in the protein shell, called the capsid. DNA condensed in this state inside viral capsids has been shown to be trapped in a glassy state, with restricted molecular motion in vitro. This limited intracapsid DNA mobility is caused by the sliding friction between closely packaged DNA strands, as a result of the repulsive interactions between the negative charges on the DNA helices. It had been unclearmore »« less
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Title: Ionic switch controls the DNA state in phage λ

Abstract

Citation Formats

Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22 journal, April 2011

Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. journal, May 1987

The effects of magnesium starvation on the ribosome content of Escherichia coli journal, June 1962

The design of an agent to bend DNA. journal, October 1996

Polyamines: Mysterious Modulators of Cellular Functions journal, May 2000

Hydration Forces book, May 2008

Challenging Packaging Limits and Infectivity of Phage journal, January 2012

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

Binding of Intercalating and Groove-Binding Cyanine Dyes to Bacteriophage T5 journal, February 2007

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

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

Kinking the double helix by bending deformation journal, December 2007

Encapsidated Conformation of Bacteriophage T7 DNA journal, October 1997

Is the In Vitro Ejection of Bacteriophage DNA Quasistatic? A Bulk to Single Virus Study journal, July 2010

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

The exchange properties of magnesium in Escherichia coli ribosomes journal, March 1964

Topological Defects and the Optimum Size of DNA Condensates journal, August 1998

Repulsion of Superinfecting Virions: A Mechanism for Rapid Virus Spread journal, January 2010

Why genes overlap in viruses journal, June 2010

Electron Microscopy of Magnesium-Depleted Bacteria journal, January 1966

Strained DNA is kinked by low concentrations of Zn2+ journal, September 1997

DNA packaging by the double-stranded DNA bacteriophages journal, September 1980

DNA bending-induced phase transition of encapsidated genome in phage λ. text, January 2013

Statics and Dynamics of Condensed DNA within Phages and Globules preprint, January 2003

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

Temperature dependence of DNA persistence length journal, October 2010

DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry journal, February 2009

Influence of Internal Capsid Pressure on Viral Infection by Phage λ journal, September 2009

DNA-DNA interactions journal, June 1998

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

Solid-To-Fluid DNA Transition Inside HSV-1 Capsid Close to the Temperature of Infection journal, January 2015

Encyclopedia of dietary supplements journal, September 2005

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

DNA bending-induced phase transition of encapsidated genome in phage λ. text, January 2013

Herpes virus genome, the pressure is on. text, January 2013

Herpes virus genome, the pressure is on. text, January 2013

Sequestered end products and enzyme regulation: the case of ornithine decarboxylase. journal, January 1992

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

Molecular biology: DNA bending and kinking journal, May 1984

Microbial magnesium transport: unusual transporters searching for identity journal, April 1998

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

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

DNA arrangement in isometric phage heads journal, August 1977

Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization journal, August 2012

Forces Controlling the Rate of DNA Ejection from Phage λ journal, April 2007

Statics and dynamics of condensed DNA within phages and globules journal, July 2004

Heat Induced Capsid Disassembly and DNA Release of Bacteriophage λ journal, July 2012

Secondary structure and interactions of the packaged dsDNA genome of bacteriophage P22 investigated by Raman difference spectroscopy journal, December 1992

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

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

Hydration Forces journal, October 1993

Exact theory of kinkable elastic polymers text, January 2004

DNA packaging and ejection forces in bacteriophage journal, November 2001

The effects of magnesium starvation on the ribosome content of Escherichia coli journal, June 1962

Mechanistic Insight into the Structure and Dynamics of Entangled and Hydrated λ-Phage DNA journal, April 2012

Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22 journal, May 2011

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

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

Temperature Dependence of DNA Persistence Length journal, February 2011

The Bacteriophage Genome Undergoes a Succession of Intracapsid Phase Transitions upon DNA Ejection journal, February 2010

Incomplete Ion Dissociation Underlies the Weakened Attraction between DNA Helices at High Spermidine Concentrations journal, September 2005

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

Condensed phases of DNA: Structures and phase transitions journal, January 1996

The effect of genome length on ejection forces in bacteriophage lambda journal, May 2006

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

Cro regulatory protein specified by bacteriophage lambda. Structure, DNA-binding, and repression of RNA synthesis. journal, September 1977

Magnesium Transport in Escherichia coli journal, May 1971

Magnesium and the Growth of Escherichia coli journal, May 1968

The Intracellular Concentration of Bound and Unbound Magnesium Ions in Escherichia coli journal, August 1967

Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. journal, May 1987

Polyamines: Mysterious Modulators of Cellular Functions journal, May 2000

DNA packaging by the double-stranded DNA bacteriophages journal, September 1980

DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry journal, February 2009

Influence of Internal Capsid Pressure on Viral Infection by Phage λ journal, September 2009

Temperature Dependence of DNA Persistence Length journal, February 2011

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

Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22
journal, April 2011

Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples.
journal, May 1987

The effects of magnesium starvation on the ribosome content of Escherichia coli
journal, June 1962

The design of an agent to bend DNA.
journal, October 1996

Polyamines: Mysterious Modulators of Cellular Functions
journal, May 2000

Hydration Forces
book, May 2008

Challenging Packaging Limits and Infectivity of Phage
journal, January 2012

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

Binding of Intercalating and Groove-Binding Cyanine Dyes to Bacteriophage T5
journal, February 2007

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

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

Kinking the double helix by bending deformation
journal, December 2007

Encapsidated Conformation of Bacteriophage T7 DNA
journal, October 1997

Is the In Vitro Ejection of Bacteriophage DNA Quasistatic? A Bulk to Single Virus Study
journal, July 2010

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

The exchange properties of magnesium in Escherichia coli ribosomes
journal, March 1964

Topological Defects and the Optimum Size of DNA Condensates
journal, August 1998

Repulsion of Superinfecting Virions: A Mechanism for Rapid Virus Spread
journal, January 2010

Why genes overlap in viruses
journal, June 2010

Electron Microscopy of Magnesium-Depleted Bacteria
journal, January 1966

Strained DNA is kinked by low concentrations of Zn2+
journal, September 1997

DNA packaging by the double-stranded DNA bacteriophages
journal, September 1980

DNA bending-induced phase transition of encapsidated genome in phage λ.
text, January 2013

Statics and Dynamics of Condensed DNA within Phages and Globules
preprint, January 2003

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

Temperature dependence of DNA persistence length
journal, October 2010

DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry
journal, February 2009

Influence of Internal Capsid Pressure on Viral Infection by Phage λ
journal, September 2009

DNA-DNA interactions
journal, June 1998

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

Solid-To-Fluid DNA Transition Inside HSV-1 Capsid Close to the Temperature of Infection
journal, January 2015

Encyclopedia of dietary supplements
journal, September 2005

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

DNA bending-induced phase transition of encapsidated genome in phage λ.
text, January 2013

Herpes virus genome, the pressure is on.
text, January 2013

Herpes virus genome, the pressure is on.
text, January 2013

Sequestered end products and enzyme regulation: the case of ornithine decarboxylase.
journal, January 1992

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

Molecular biology: DNA bending and kinking
journal, May 1984

Microbial magnesium transport: unusual transporters searching for identity
journal, April 1998

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

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

DNA arrangement in isometric phage heads
journal, August 1977

Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization
journal, August 2012

Forces Controlling the Rate of DNA Ejection from Phage λ
journal, April 2007

Statics and dynamics of condensed DNA within phages and globules
journal, July 2004

Heat Induced Capsid Disassembly and DNA Release of Bacteriophage λ
journal, July 2012

Secondary structure and interactions of the packaged dsDNA genome of bacteriophage P22 investigated by Raman difference spectroscopy
journal, December 1992

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

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

Hydration Forces
journal, October 1993

Exact theory of kinkable elastic polymers
text, January 2004

DNA packaging and ejection forces in bacteriophage
journal, November 2001

The effects of magnesium starvation on the ribosome content of Escherichia coli
journal, June 1962

Mechanistic Insight into the Structure and Dynamics of Entangled and Hydrated λ-Phage DNA
journal, April 2012

Peering Down the Barrel of a Bacteriophage Portal: The Genome Packaging and Release Valve in P22
journal, May 2011

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

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

Temperature Dependence of DNA Persistence Length
journal, February 2011

The Bacteriophage Genome Undergoes a Succession of Intracapsid Phase Transitions upon DNA Ejection
journal, February 2010

Incomplete Ion Dissociation Underlies the Weakened Attraction between DNA Helices at High Spermidine Concentrations
journal, September 2005

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

Condensed phases of DNA: Structures and phase transitions
journal, January 1996

The effect of genome length on ejection forces in bacteriophage lambda
journal, May 2006

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

Cro regulatory protein specified by bacteriophage lambda. Structure, DNA-binding, and repression of RNA synthesis.
journal, September 1977

Magnesium Transport in Escherichia coli
journal, May 1971

Magnesium and the Growth of Escherichia coli
journal, May 1968

The Intracellular Concentration of Bound and Unbound Magnesium Ions in Escherichia coli
journal, August 1967

Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples.
journal, May 1987

Polyamines: Mysterious Modulators of Cellular Functions
journal, May 2000

DNA packaging by the double-stranded DNA bacteriophages
journal, September 1980

DNA Heats Up: Energetics of Genome Ejection from Phage Revealed by Isothermal Titration Calorimetry
journal, February 2009

Influence of Internal Capsid Pressure on Viral Infection by Phage λ
journal, September 2009

Temperature Dependence of DNA Persistence Length
journal, February 2011

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

Forces Controlling the Rate of DNA Ejection from Phage λ
journal, April 2007

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

Spontaneous Sharp Bending of Double-Stranded DNA
journal, May 2004