A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells

Elife. 2014 Nov 27:3:e03197. doi: 10.7554/eLife.03197.

Abstract

Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to position DNA at mid-cell, without which infectivity is compromised. Here, we show that PhuZ filaments, like microtubules, stochastically switch from growing in a distinctly polar manner to catastrophic depolymerization (dynamic instability) both in vitro and in vivo. One end of each PhuZ filament is stably anchored near the cell pole to form a spindle-like array that orients the growing ends toward the phage nucleoid so as to position it near mid-cell. Our results demonstrate how a bacteriophage can harness the properties of a tubulin-like cytoskeleton for efficient propagation. This represents the first identification of a prokaryotic tubulin with the dynamic instability of microtubules and the ability to form a simplified bipolar spindle.

Keywords: bacteriophage; cell biology; cytoskeleton; dynamic instability; pseudomonas; spindle; tubulin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriophages / metabolism*
  • DNA Replication
  • DNA, Viral / metabolism*
  • Hydrolysis
  • In Situ Hybridization, Fluorescence
  • Microscopy, Fluorescence
  • Models, Biological
  • Nucleotides / metabolism
  • Polymerization
  • Spindle Apparatus / metabolism
  • Time-Lapse Imaging
  • Tubulin / metabolism*
  • Viral Proteins / metabolism*

Substances

  • DNA, Viral
  • Nucleotides
  • Tubulin
  • Viral Proteins