Quantitative Study of the Chiral Organization of the Phage Genome Induced by the Packaging Motor

Molecular motors that translocate DNA are ubiquitous in nature. During morphogenesis of double-stranded DNA bacteriophages, a molecular motor drives the viral genome inside a protein capsid. Several models have been proposed for the three-dimensional geometry of the packaged genome, but very little is known of the signature of the molecular packaging motor. For instance, biophysical experiments show that in some systems, DNA rotates during the packaging reaction, but most current biophysical models fail to incorporate this property. Furthermore, studies including rotation mechanisms have reached contradictory conclusions. In this study, we compare the geometrical signatures imposed by different possible mechanisms for the packaging motors: rotation, revolution, and rotation with revolution. We used a previously proposed kinetic Monte Carlo model of the motor, combined with Brownian dynamics simulations of DNA to simulate deterministic and stochastic motor models. We find that rotation is necessary for the accumulation of DNA writhe and for the chiral organization of the genome. We observe that although in the initial steps of the packaging reaction, the torsional strain of the genome is released by rotation of the molecule, in the later stages, it is released by the accumulation of writhe. We suggest that the molecular motor plays a key role in determining the final structure of the encapsidated genome in bacteriophages. SIGNIFICANCE The three-dimensional organization of viral genomes determines key functional aspects of viral infection. In double-stranded DNA bacteriophages, the packaging reaction is carried out by a molecular motor that drives the viral genome inside its protein capsid. In this study, we determine the contribution of the packaging motor to the final packaged configuration of the viral genome. Using a previously proposed kinetic Monte Carlo model of the motor, combined with Brownian dynamics simulations of DNA, we find that rotation of the DNA molecule by the motor during the packaging reaction induces chiral packing.