Characterization of a lipid-based jumbo phage compartment as a hub for early phage infection

Cell Host Microbe. 2024 Jul 10;32(7):1050-1058.e7. doi: 10.1016/j.chom.2024.05.016. Epub 2024 Jun 12.

Abstract

Viral genomes are most vulnerable to cellular defenses at the start of the infection. A family of jumbo phages related to phage ΦKZ, which infects Pseudomonas aeruginosa, assembles a protein-based phage nucleus to protect replicating phage DNA, but how it is protected prior to phage nucleus assembly is unclear. We find that host proteins related to membrane and lipid biology interact with injected phage protein, clustering in an early phage infection (EPI) vesicle. The injected virion RNA polymerase (vRNAP) executes early gene expression until phage genome separation from the vRNAP and the EPI vesicle, moving into the nascent proteinaceous phage nucleus. Enzymes involved in DNA replication and CRISPR/restriction immune nucleases are excluded by the EPI vesicle. We propose that the EPI vesicle is rapidly constructed with injected phage proteins, phage DNA, host lipids, and host membrane proteins to enable genome protection, early transcription, localized translation, and to ensure faithful genome transfer to the proteinaceous nucleus.

Keywords: Chimallinviridae; bacteria-phage cell biology; bacterial fluorescence microscopy; bacteriophage; jumbo phage; lipid vesicle; phage nucleus; proteomics.

MeSH terms

  • Bacteriophages / genetics
  • Bacteriophages / physiology
  • DNA Replication
  • DNA, Viral* / genetics
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism
  • Genome, Viral*
  • Lipids
  • Pseudomonas Phages* / genetics
  • Pseudomonas Phages* / metabolism
  • Pseudomonas aeruginosa* / virology
  • Viral Proteins / genetics
  • Viral Proteins / metabolism
  • Virion / metabolism
  • Virus Replication

Substances

  • DNA, Viral
  • Viral Proteins
  • DNA-Directed RNA Polymerases
  • Lipids