Shape shifter: redirection of prolate phage capsid assembly by staphylococcal pathogenicity islands

Phage-inducible chromosomal islands (PICIs) are a group of mobile genetic elements that hijack the replication and assembly machinery of helper bacteriophages. Here the authors describe a mechanism by which a group of PICIs from Staphylococcus aureus re-direct the assembly pathway of their helpers using a capsid protein homolog. Staphylococcus aureus pathogenicity islands (SaPIs) are molecular parasites that hijack helper phages for their transfer. SaPIbov5, the prototypical member of a family of cos type SaPIs, redirects the assembly of phi 12 helper capsids from prolate to isometric. This size and shape shift is dependent on the SaPIbov5-encoded protein Ccm, a homolog of the phi 12 capsid protein (CP). Using cryo-electron microscopy, we have determined structures of prolate phi 12 procapsids and isometric SaPIbov5 procapsids. phi 12 procapsids have icosahedral end caps with T-end = 4 architecture and a T-mid = 14 cylindrical midsection, whereas SaPIbov5 procapsids have T = 4 icosahedral architecture. We built atomic models for CP and Ccm, and show that Ccm occupies the pentameric capsomers in the isometric SaPIbov5 procapsids, suggesting that preferential incorporation of Ccm pentamers prevents the cylindrical midsection from forming. Our results highlight that pirate elements have evolved diverse mechanisms to suppress phage multiplication, including the acquisition of phage capsid protein homologs.

Automated summary

Phage-inducible chromosomal islands (PICIs) are mobile genetic elements that hijack helper bacteriophages' replication and assembly machinery. Staphylococcus aureus pathogenicity islands (SaPIs), such as SaPIbov5, redirect the assembly pathway of their helper phages by introducing a capsid protein homolog, Ccm. Cryo-electron microscopy studies show that Ccm occupies the pentameric capsomers in SaPIbov5 procapsids, preventing the formation of the cylindrical midsection seen in typical phage procapsids.