Abstract
Icosahedral double-stranded DNA viruses use a single portal for genome delivery and packaging. The extensive structural similarity revealed by such portals in diverse viruses, as well as their invariable positioning at a unique icosahedral vertex, led to the consensus that a particular, highly conserved vertex-portal architecture is essential for viral DNA translocations. Here we present an exception to this paradigm by demonstrating that genome delivery and packaging in the virus Acanthamoeba polyphaga mimivirus occur through two distinct portals. By using high-resolution techniques, including electron tomography and cryo-scanning electron microscopy, we show that Mimivirus genome delivery entails a large-scale conformational change of the capsid, whereby five icosahedral faces open up. This opening, which occurs at a unique vertex of the capsid that we coined the “stargate”, allows for the formation of a massive membrane conduit through which the viral DNA is released. A transient aperture centered at an icosahedral face distal to the DNA delivery site acts as a non-vertex DNA packaging portal. In conjunction with comparative genomic studies, our observations imply a viral packaging pathway akin to bacterial DNA segregation, which might be shared by diverse internal membrane–containing viruses.
Highlights
The prevailing model for genome translocations in icosahedral viruses entails a molecular motor that is localized at a single vertex and comprises a packaging ATPase and a portal complex [1,2,3,4,5]
By performing cryo-scanning electron microscopy and electron tomography on cryo-preserved host cells at different post-infection time points, we demonstrate that DNA exit occurs in phagosome-enclosed viral particles through a massive opening of five icosahedral faces of the capsid
We have addressed the question of whether such a linear translocation through a single portal takes place for viruses harboring very large genomes, by studying genome delivery and packaging in the amoeba-infecting virus Acanthamoeba polyphaga mimivirus
Summary
The prevailing model for genome translocations in icosahedral viruses entails a molecular motor that is localized at a single vertex and comprises a packaging ATPase and a portal complex [1,2,3,4,5]. Vertex-portal assemblies were, characterized only in herpesviruses that contain an external lipid membrane [3,4,10], and in tailed double-stranded DNA (dsDNA) bacteriophages in which membranes are absent [1,5,6,7,11]. This point is noteworthy in light of recent studies, which implied that DNA packaging machinery in viruses containing an inner membrane layer is fundamentally different from the vertex-portal apparatus of herpesviruses and bacteriophages [12,13,14]. The structural aspects that underlie genome translocation mechanisms deployed by these viruses remain, largely unknown [15]
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