Structural dynamics of bacteriophage P22 infection initiation revealed by cryo-electron tomography

• Published in: Nature microbiology Vol. 4; no. 6; pp. 1049 - 1056
• Main Authors: Wang, Chunyan, Tu, Jiagang, Liu, Jun, Molineux, Ian J.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2019; Nature Publishing Group
• Subjects: 101/28; 38/44; 631/326; 631/535; Bacteriophage P22 - pathogenicity; Bacteriophage P22 - physiology; Bacteriophage P22 - ultrastructure; Biomedical and Life Sciences; Cell Membrane - metabolism; Cell Membrane - ultrastructure; Cell Membrane - virology; Cell surface; Cytoplasm; Cytoplasm - metabolism; Cytoplasm - virology; DNA, Viral; Electron Microscope Tomography - methods; Genomes; Gram-negative bacteria; Infections; Infectious Diseases; Life Sciences; Medical Microbiology; Microbiology; Models, Molecular; O antigen; O Antigens; Parasitology; Periplasm; Phages; Protein Conformation; Proteins; Salmonella enterica; Salmonella typhimurium - virology; Tomography; Viral Tail Proteins - chemistry; Virion - metabolism; Virions; Virology; Virus Attachment; Virus Internalization
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-019-0403-z

For successful infection, bacteriophages must overcome multiple barriers to transport their genome and proteins across the bacterial cell envelope. We use cryo-electron tomography to study the infection initiation of phage P22 in Salmonella enterica serovar Typhimurium, revealing how a channel forms to allow genome translocation into the cytoplasm. Our results show free phages that initially attach obliquely to the cell through interactions between the O antigen and two of the six tailspikes; the tail needle also abuts the cell surface. The virion then orients perpendicularly and the needle penetrates the outer membrane. The needle is released and the internal head protein gp7* is ejected and assembles into an extracellular channel that extends from the gp10 baseplate to the cell surface. A second protein, gp20, is ejected and assembles into a structure that extends the extracellular channel across the outer membrane into the periplasm. Insertion of the third ejected protein, gp16, into the cytoplasmic membrane probably completes the overall trans-envelope channel into the cytoplasm. Construction of a trans-envelope channel is an essential step during infection of Gram-negative bacteria by all short-tailed phages, because such virions cannot directly deliver their genome into the cell cytoplasm. Cryo-electron tomography was used to study the initial steps of infection of Salmonella enterica serovar Salmonella Typhimurium with phage P22 and reveals how the phage forms a channel through the host outer and inner membranes to translocate its genome into the bacterial cytoplasm.