Double-stranded DNA organization in bacteriophage heads: an alternative toroid-based model

Abstract

Studies of the organization of double-stranded DNA within bacteriophage heads during the past four decades have produced a wealth of data. However, despite the presentation of numerous models, the true organization of DNA within phage heads remains unresolved. The observations of toroidal DNA structures in electron micrographs of phage lysates have long been cited as support for the organization of DNA in a spool-like fashion. This particular model, like all other models, has not been found to be consistent will all available data. Recently we proposed that DNA within toroidal condensates produced in vitro is organized in a manner significantly different from that suggested by the spool model. This new toroid model has allowed the development of an alternative model for DNA organization within bacteriophage heads that is consistent with a wide range of biophysical data. Here we propose that bacteriophage DNA is packaged in a toroid that is folded into a highly compact structure.

The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape

“…Arrangement of the DNA along the long axis was not considered in earlier theoretical work (Purohit et al, 2005), presumably because it was unclear what global structure would permit this. The folded toroid, first proposed by Nicholas Hud (Hud, 1995) solves this problem.…”

“…These led to the coaxial spool model (Richards et al, 1973), which remains the most widely-accepted model for DNA in icosahedral capsids. Other models include the ball of string (Earnshaw and Harrison, 1977), the folded chain (Earnshaw and Harrison, 1977), the interwound toroid (Earnshaw et al, 1978), toroidal winding (Kosturko et al, 1979), the kinked chain (Serwer, 1986), and the folded toroid (Hud, 1995).…”

DNA knots reveal a chiral organization of DNA in phage capsids

“…Many studies have found that regions of the packed DNA form domains of parallel fibers, which in some cases have different orientations, suggesting a certain degree of randomness (8,9,13,14). The above observations have led to the proposal of several long-range organization models for DNA inside phage capsids: the ball of string model (13), the coaxial spooling model (8,11,13,14), the spiral-fold model (15), and the folded toroidal model (16). Liquid crystalline models, which take into account properties of DNA at high concentrations and imply less global organization, have also been proposed (9).…”

Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids

“…In the ''mature'' P4 phages (i.e., complete infective particles with capsid and tail), one of the two cohesive ends of the DNA is known to remain anchored near the connector region (19), while the bulk of packed DNA plus its associated water molecules virtually occupy the total volume of the capsid (20). Despite the system's apparent simplicity, the overall arrangement of the DNA inside the viral capsid remains largely unknown (21)(22)(23)(24)(25).…”