A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills.
Multimeric, ring-shaped molecular motors rely on the coordinated action of their subunits to perform crucial biological functions. During these tasks, motors often change their operation in response to regulatory signals. Here, we investigate a viral packaging machine as it fills the capsid with DNA and encounters increasing internal pressure. We find that the motor rotates the DNA during packaging and that the rotation per base pair increases with filling. This change accompanies a reduction in the motor's step size. We propose that these adjustments preserve motor coordination by allowing one subunit to make periodic, specific, and regulatory contacts with the DNA. At high filling, we also observe the downregulation of the ATP-binding rate and the emergence of long-lived pauses, suggesting a throttling-down mechanism employed by the motor near the completion of packaging. This study illustrates how a biological motor adjusts its operation in response to changing conditions, while remaining highly coordinated.
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|California Institute for Quantitative Biosciences University of California, Berkeley, CA 94720, USA.
Shixin
S
Liu
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|Department of Physics University of California, Berkeley, CA 94720, USA.
Gheorghe
G
Chistol
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|California Institute for Quantitative Biosciences University of California, Berkeley, CA 94720, USA.|Department of Physics University of California, Berkeley, CA 94720, USA.
Craig L
CL
Hetherington
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|Biophysics Graduate Group University of California, Berkeley, CA 94720, USA.
Sara
S
Tafoya
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|Biophysics Graduate Group University of California, Berkeley, CA 94720, USA.
K
K
Aathavan
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|California Institute for Quantitative Biosciences University of California, Berkeley, CA 94720, USA.
Joerg
J
Schnitzbauer
Department of Diagnostic and Biological Sciences and Institute for Molecular Virology, University of Minnesota, Minneapolis, MN 55455, USA.
Shelley
S
Grimes
Department of Diagnostic and Biological Sciences and Institute for Molecular Virology, University of Minnesota, Minneapolis, MN 55455, USA.
Paul J
PJ
Jardine
Jason L. Choy Laboratory of Single Molecule Biophysics University of California, Berkeley, CA 94720, USA.|California Institute for Quantitative Biosciences University of California, Berkeley, CA 94720, USA.|Department of Physics University of California, Berkeley, CA 94720, USA.|Department of Molecular and Cell Biology, Department of Chemistry, and Howard Hughes Medical Institute, University of California, Berkeley, CA 94720, USA.|Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.|Kavli Energy NanoSciences Institute at the University of California, Berkeley and the Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Carlos
C
Bustamante
D000255:Adenosine Triphosphate / Q000378:metabolism; D017103:Bacillus Phages / Q000502:physiology*; D002213:Capsid / Q000737:chemistry; D004279:DNA, Viral / Q000378:metabolism; D020409:Molecular Motor Proteins / Q000378:metabolism*; D014764:Viral Proteins / Q000378:metabolism*; D019065:Virus Assembly
D004279:DNA, Viral; D020409:Molecular Motor Proteins; D014764:Viral Proteins; D000255:Adenosine Triphosphate