The architecture and stabilisation of flagellotropic tailed bacteriophages

Joshua M Hardy,Hariprasad Venugopal,Gordon Dougan,Rhys Grinter,Rhys A Dunstan,Fasséli Coulibaly,Matthew J Belousoff,Jiawei Wang,Trevor Lithgow,Derek Pickard

doi:10.1038/s41467-020-17505-w

Abstract

Flagellotropic bacteriophages engage flagella to reach the bacterial surface as an effective means to increase the capture radius for predation. Structural details of these viruses are of great interest given the substantial drag forces and torques they face when moving down the spinning flagellum. We show that the main capsid and auxiliary proteins form two nested chainmails that ensure the integrity of the bacteriophage head. Core stabilising structures are conserved in herpesviruses suggesting their ancestral origin. The structure of the tail also reveals a robust yet pliable assembly. Hexameric rings of the tail-tube protein are braced by the N-terminus and a β-hairpin loop, and interconnected along the tail by the splayed β-hairpins. By contrast, we show that the β-hairpin has an inhibitory role in the tail-tube precursor, preventing uncontrolled self-assembly. Dyads of acidic residues inside the tail-tube present regularly-spaced motifs well suited to DNA translocation into bacteria through the tail.

Highlights

Flagellotropic bacteriophages engage flagella to reach the bacterial surface as an effective means to increase the capture radius for predation
We have determined by cryo-electron microscopy structures of the head and tail components of YSD1, a phage infecting Salmonella Typhi
The architecture of the YSD1 head and tail components sheds light on assembly strategies and stabilising features that are conserved beyond the λ/χ-like phages

Summary

Introduction

Flagellotropic bacteriophages engage flagella to reach the bacterial surface as an effective means to increase the capture radius for predation. In contractile tails of myoviruses, an outer sheath braces the entire central tailtube in the pre-contracted state, presumably adding stability to the assembly Given that they have no outer tube structure and are up to twice as long, it is of interest to understand how tailtube integrity is maintained in flexible tails typical of the Siphoviridae. At a resolution of 3.8 Å, the structure of the YSD1 head provides a model for the λ/χ-like capsids presenting unique similarities with herpesvirus virions These capsids share an external non-covalent chainmail of the auxiliary protein, which adds to the stability of the particle. The 3.5 Å-resolution structure of the YSD1 tail reveals a robust but pliable assembly based on hexameric rings strung around a central spine of the tape measure protein. An extended β-hairpin plays a dual role in assembly, mediating most of the inter-ring contacts in the assembled tail but preventing uncontrolled selfassembly of the tail-tube precursor

Methods

Results

Conclusion