A cytoskeletal vortex drives phage nucleus rotation during jumbo phage replication in E. coli

SUMMARY

Nucleus-forming jumbo phages establish an intricate subcellular organization, enclosing phage genomes within a proteinaceous shell called the phage nucleus. During infection in Pseudomonas, some jumbo phages assemble a bipolar spindle of tubulin-like PhuZ filaments that positions the phage nucleus at midcell and drives its intracellular rotation. This facilitates the distribution of capsids on its surface for genome packaging. Here we show that the Escherichia coli jumbo phage Goslar assembles a phage nucleus surrounded by an array of PhuZ filaments resembling a vortex instead of a bipolar spindle. Expression of a mutant PhuZ protein strongly reduces Goslar phage nucleus rotation, demonstrating that the PhuZ cytoskeletal vortex is necessary for rotating the phage nucleus. While vortex-like cytoskeletal arrays are important in eukaryotes for cytoplasmic streaming and nucleus alignment, this work identifies a coherent assembly of filaments into a vortex-like structure driving intracellular rotation within the prokaryotic cytoplasm.

In brief

The phage nucleus was recently discovered, and the diversity and ubiquity of this phage replication pathway is unclear. Birkholz et al. identify a nucleus-forming E. coli phage and show that tubulin (PhuZ) filaments form a vortex-like structure driving intracellular rotation of the phage nucleus within the prokaryotic cytoplasm.

Graphical Abstract