Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase

Liu, Ninning; Chistol, Gheorghe; Bustamante, Carlos

doi:10.7554/eLife.09224

Title: Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase

Abstract

SpoIIIE is a homo-hexameric dsDNA translocase responsible for completing chromosome segregation in Bacillus subtilis . Here, we use a single-molecule approach to monitor SpoIIIE translocation when challenged with neutral-backbone DNA and non-hydrolyzable ATP analogs. We show that SpoIIIE makes multiple essential contacts with phosphates on the 5'→3' strand in the direction of translocation. Using DNA constructs with two neutral-backbone segments separated by a single charged base pair, we deduce that SpoIIIE’s step size is 2 bp. Finally, experiments with non-hydrolyzable ATP analogs suggest that SpoIIIE can operate with non-consecutive inactive subunits. We propose a two-subunit escort translocation mechanism that is strict enough to enable SpoIIIE to track one DNA strand, yet sufficiently compliant to permit the motor to bypass inactive subunits without arrest. We speculate that such a flexible mechanism arose for motors that, like SpoIIIE, constitute functional bottlenecks where the inactivation of even a single motor can be lethal for the cell.

Authors:: Liu, Ninning; Chistol, Gheorghe; Bustamante, Carlos

Publication Date:: Fri Oct 09 00:00:00 EDT 2015

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)

OSTI Identifier:: 1233979

Alternate Identifier(s):: OSTI ID: 1233980; OSTI ID: 1415944

Grant/Contract Number:: AC02-05CH11231; R01GM071552; R01GM032543

Resource Type:: Published Article

Journal Name:: eLife

Additional Journal Information:: Journal Name: eLife Journal Volume: 4; Journal ID: ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Liu, Ninning, Chistol, Gheorghe, and Bustamante, Carlos. Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase.  United States: N. p., 2015. 
Web.  doi:10.7554/eLife.09224.

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                    Liu, Ninning, Chistol, Gheorghe, & Bustamante, Carlos. Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase.  United States.  https://doi.org/10.7554/eLife.09224

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                    Liu, Ninning, Chistol, Gheorghe, and Bustamante, Carlos. Fri .  
"Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase".  United States.  https://doi.org/10.7554/eLife.09224.

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@article{osti_1233979,

  title        = {Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase},

  author       = {Liu, Ninning and Chistol, Gheorghe and Bustamante, Carlos},

  abstractNote = {SpoIIIE is a homo-hexameric dsDNA translocase responsible for completing chromosome segregation in Bacillus subtilis . Here, we use a single-molecule approach to monitor SpoIIIE translocation when challenged with neutral-backbone DNA and non-hydrolyzable ATP analogs. We show that SpoIIIE makes multiple essential contacts with phosphates on the 5'→3' strand in the direction of translocation. Using DNA constructs with two neutral-backbone segments separated by a single charged base pair, we deduce that SpoIIIE’s step size is 2 bp. Finally, experiments with non-hydrolyzable ATP analogs suggest that SpoIIIE can operate with non-consecutive inactive subunits. We propose a two-subunit escort translocation mechanism that is strict enough to enable SpoIIIE to track one DNA strand, yet sufficiently compliant to permit the motor to bypass inactive subunits without arrest. We speculate that such a flexible mechanism arose for motors that, like SpoIIIE, constitute functional bottlenecks where the inactivation of even a single motor can be lethal for the cell.},

  doi          = {10.7554/eLife.09224},

  journal      = {eLife},

  number       = ,

  volume       = 4,

  place        = {United States},

  year         = {Fri Oct 09 00:00:00 EDT 2015},

  month        = {Fri Oct 09 00:00:00 EDT 2015}

}

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Similar Records

Title: Two-subunit DNA escort mechanism and inactive subunit bypass in an ultra-fast ring ATPase

Abstract

Citation Formats

FtsK and SpoIIIE: the tale of the conserved tails journal, December 2007

Separating speed and ability to displace roadblocks during DNA translocation by FtsK journal, April 2010

Molecular Mechanism of Sequence-Directed DNA Loading and Translocation by FtsK journal, August 2008

Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase journal, November 2005

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis journal, April 2008

Sequence-Directed DNA Translocation by Purified FtsK journal, January 2005

Identification of the FtsK sequence-recognition domain journal, October 2006

FtsK: a groovy helicase journal, November 2006

Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment journal, May 2004

The Structure of the Phage T4 DNA Packaging Motor Suggests a Mechanism Dependent on Electrostatic Forces journal, December 2008

Stochastic but Highly Coordinated Protein Unfolding and Translocation by the ClpXP Proteolytic Machine journal, July 2014

Structure and DNA-binding properties of the Bacillus subtilis SpoIIIE DNA translocase revealed by single-molecule and electron microscopies journal, November 2013

When a helicase is not a helicase: dsDNA tracking by the motor protein EcoR124I journal, April 2006

Double-Stranded DNA Translocation: Structure and Mechanism of Hexameric FtsK journal, August 2006

Substrate interactions and promiscuity in a viral DNA packaging motor journal, October 2009

Role of Bacillus subtilis SpoIIIE in DNA Transport Across the Mother Cell-Prespore Division Septum journal, November 2000

Sequence-specific assembly of FtsK hexamers establishes directional translocation on DNA journal, November 2010

Nucleosomal Fluctuations Govern the Transcription Dynamics of RNA Polymerase II journal, July 2009

SpoIIIE strips proteins off the DNA during chromosome translocation journal, July 2008

SpoIIIE mechanism of directional translocation involves target search coupled to sequence-dependent motor stimulation journal, April 2013

High Degree of Coordination and Division of Labor among Subunits in a Homomeric Ring ATPase journal, November 2012

The ClpXP Protease Unfolds Substrates Using a Constant Rate of Pulling but Different Gears journal, October 2013

Ionic effects on the elasticity of single DNA molecules journal, June 1997

Dramatic increase in negative superhelicity of plasmid DNA in the forespore compartment of sporulating cells of Bacillus subtilis. journal, January 1990

Running in Reverse: The Structural Basis for Translocation Polarity in Hexameric Helicases journal, October 2009

Helical repeat of DNA in solution. journal, January 1979

Mechanism of DNA translocation in a replicative hexameric helicase journal, July 2006

A Viral Packaging Motor Varies Its DNA Rotation and Step Size to Preserve Subunit Coordination as the Capsid Fills journal, April 2014

The bacteriophage φ29 portal motor can package DNA against a large internal force journal, October 2001

Visualization and functional dissection of coaxial paired SpoIIIE channels across the sporulation septum journal, May 2015

SpoIIIE Protein Achieves Directional DNA Translocation through Allosteric Regulation of ATPase Activity by an Accessory Domain journal, August 2013

Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking journal, April 2005

Single-Molecule Imaging of FtsK Translocation Reveals Mechanistic Features of Protein-Protein Collisions on DNA journal, June 2014

DNA bending by asymmetric phosphate neutralization journal, December 1994

Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK journal, April 2012

The Hexameric Helicase DnaB Adopts a Nonplanar Conformation during Translocation journal, October 2012

Bacillus subtilis spoIIIE protein required for DNA segregation during asymmetric cell division journal, April 1994

The nuts and bolts of ring-translocase structure and mechanism journal, April 2011

The ATPase SpoIIIE Transports DNA across Fused Septal Membranes during Sporulation in Bacillus subtilis journal, December 2007

FtsK and SpoIIIE: the tale of the conserved tails
journal, December 2007

Separating speed and ability to displace roadblocks during DNA translocation by FtsK
journal, April 2010

Molecular Mechanism of Sequence-Directed DNA Loading and Translocation by FtsK
journal, August 2008

Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase
journal, November 2005

Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis
journal, April 2008

Sequence-Directed DNA Translocation by Purified FtsK
journal, January 2005

Identification of the FtsK sequence-recognition domain
journal, October 2006

FtsK: a groovy helicase
journal, November 2006

Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment
journal, May 2004

The Structure of the Phage T4 DNA Packaging Motor Suggests a Mechanism Dependent on Electrostatic Forces
journal, December 2008

Stochastic but Highly Coordinated Protein Unfolding and Translocation by the ClpXP Proteolytic Machine
journal, July 2014

Structure and DNA-binding properties of the Bacillus subtilis SpoIIIE DNA translocase revealed by single-molecule and electron microscopies
journal, November 2013

When a helicase is not a helicase: dsDNA tracking by the motor protein EcoR124I
journal, April 2006

Double-Stranded DNA Translocation: Structure and Mechanism of Hexameric FtsK
journal, August 2006

Substrate interactions and promiscuity in a viral DNA packaging motor
journal, October 2009

Role of Bacillus subtilis SpoIIIE in DNA Transport Across the Mother Cell-Prespore Division Septum
journal, November 2000

Sequence-specific assembly of FtsK hexamers establishes directional translocation on DNA
journal, November 2010

Nucleosomal Fluctuations Govern the Transcription Dynamics of RNA Polymerase II
journal, July 2009

SpoIIIE strips proteins off the DNA during chromosome translocation
journal, July 2008

SpoIIIE mechanism of directional translocation involves target search coupled to sequence-dependent motor stimulation
journal, April 2013

High Degree of Coordination and Division of Labor among Subunits in a Homomeric Ring ATPase
journal, November 2012

The ClpXP Protease Unfolds Substrates Using a Constant Rate of Pulling but Different Gears
journal, October 2013

Ionic effects on the elasticity of single DNA molecules
journal, June 1997

Dramatic increase in negative superhelicity of plasmid DNA in the forespore compartment of sporulating cells of Bacillus subtilis.
journal, January 1990

Running in Reverse: The Structural Basis for Translocation Polarity in Hexameric Helicases
journal, October 2009

Helical repeat of DNA in solution.
journal, January 1979

Mechanism of DNA translocation in a replicative hexameric helicase
journal, July 2006

A Viral Packaging Motor Varies Its DNA Rotation and Step Size to Preserve Subunit Coordination as the Capsid Fills
journal, April 2014

The bacteriophage φ29 portal motor can package DNA against a large internal force
journal, October 2001

Visualization and functional dissection of coaxial paired SpoIIIE channels across the sporulation septum
journal, May 2015

SpoIIIE Protein Achieves Directional DNA Translocation through Allosteric Regulation of ATPase Activity by an Accessory Domain
journal, August 2013

Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking
journal, April 2005

Single-Molecule Imaging of FtsK Translocation Reveals Mechanistic Features of Protein-Protein Collisions on DNA
journal, June 2014

DNA bending by asymmetric phosphate neutralization
journal, December 1994

Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK
journal, April 2012

The Hexameric Helicase DnaB Adopts a Nonplanar Conformation during Translocation
journal, October 2012

Bacillus subtilis spoIIIE protein required for DNA segregation during asymmetric cell division
journal, April 1994

The nuts and bolts of ring-translocase structure and mechanism
journal, April 2011

The ATPase SpoIIIE Transports DNA across Fused Septal Membranes during Sporulation in Bacillus subtilis
journal, December 2007