The structure of a thermostable phage’s Portal Vertex and Neck Complex illuminates its maturation process

Nearly all viruses use a proteinaceous capsid shell to protect their genome. In tailed bacteriophages and herpesviruses, the genome is packaged through the conserved Portal complex, a dodecameric ring embedded in the capsid at a single vertex. After genome packaging is complete, the Portal complex connects to the Tail, which is required for host recognition and infection. Portal and the proteins that connect it to the Tail form the Neck complex, which controls genome retention in the capsid. We determined the Neck and Portal Vertex structure of the hyperthermophilic phage P74-26 using cryo-Electron Microscopy (cryo-EM). Because this phage inhabits an extremely harsh environment, it is an excellent model to study principles of thermostability and viral maturation. We describe a thermostability mechanism wherein the Portal Vertex is stabilized by highly intertwined loop structures, like in a wicker basket. Moreover, by comparing the mature virion Neck to published structures of procapsids and empty mature capsids, we observe that the Portal protrudes from the capsid upon completion of genome packaging. We propose that this repositioning of the Portal underlies a pressure-sensitive switch that terminates genome packaging and triggers Tail attachment in many phages.