Conserved and Diverse Traits of Adhesion Devices from Siphoviridae Recognizing Proteinaceous or Saccharidic Receptors

Abstract

Bacteriophages can play beneficial roles in phage therapy and destruction of food pathogens. Conversely, they play negative roles as they infect bacteria involved in fermentation, resulting in serious industrial losses. Siphoviridae phages possess a long non-contractile tail and use a mechanism of infection whose first step is host recognition and binding. They have evolved adhesion devices at their tails’ distal end, tuned to recognize specific proteinaceous or saccharidic receptors on the host’s surface that span a large spectrum of shapes. In this review, we aimed to identify common patterns beyond this apparent diversity. To this end, we analyzed siphophage tail tips or baseplates, evaluating their known structures, where available, and uncovering patterns with bioinformatics tools when they were not. It was thereby identified that a triad formed by three proteins in complex, i.e., the tape measure protein (TMP), the distal tail protein (Dit), and the tail-associated lysozyme (Tal), is conserved in all phages. This common scaffold may harbor various functional extensions internally while it also serves as a platform for plug-in ancillary or receptor-binding proteins (RBPs). Finally, a group of siphophage baseplates involved in saccharidic receptor recognition exhibits an activation mechanism reminiscent of that observed in Myoviridae.

Characterization of the First Virulent Phage Infecting Oenococcus oeni, the Queen of the Cellars

“…Tal (TMP+2) analysis yielded several hits ( Supplementary Figure 1 ). Contrary to most cases, the classical N-terminal structural domain found in all Tals ( Goulet et al, 2020 ) is identified by HHpred not at the N-terminus, but between residues 156 and 505 (PDB ID 3GS9, Listerial phage protein). Preceeding it, the domain comprised between amino-acids 1 and 155 in Vinitor162 is identified as Carbohydrate Binding Module 1 (CBM), a BppA (base plate protein) domain of lactococcal phage Tuc2009, a module widely spread in siphophages infecting Gram-positive hosts (PDB ID 5E7T, Legrand et al, 2016 ).…”

“…The structural components of the bacteriophage tail resembled the complex system found in a majority of characterized LAB phages, comprising a triad of proteins (gp16, tape measure protein, TMP; gp17, distal tail protein, Dit and gp18, tail associated protein, Tal) which allow the recognition and binding to host cell surface-located polysaccharides, or more rarely proteins ( Goulet et al, 2020 ). Gp16 was assigned to the TMP, which determines the length of the tail and participates in the infection mechanism.…”

Structure of the Capsid Size-Determining Scaffold of “Satellite” Bacteriophage P4

“…The most striking example of this is the conserved capsid fold across all members of the Caudovirales observed to date [38]. Other major structural proteins, like the major tail protein, the portal (connector) protein, and certain baseplate proteins are also highly conserved [46][47][48]. Presumably, this relatedness extends to scaffolding proteins as well; however, structural information on scaffolding proteins is still scarce.…”

Structural Insights into Lactococcal Siphophage p2 Baseplate Activation Mechanism

“…This phage has a genome size of 27,595 bp and 50 annotated open reading frames. Of interest here, phage p2 uses a multi-protein baseplate at the tip of its tail to bind to its cell wall polysaccharide (CWPS) receptor at the host cell surface [ 6 , 7 , 8 ].…”

“…Here, we present further structural analyzes of the phage p2 baseplate, proposing a topological model of the baseplate resting state, and interpreting a new nsEM structure of the virion, in its active conformation. These novel views on the activation mechanism of phage p2 may be applicable to other members of the Siphoviridae family exhibiting an activation mechanism [ 7 , 12 ].…”