Biogenesis of a Bacteriophage Long Non-Contractile Tail

• Published in: Journal of molecular biology 2021-09, Vol.433 (18), p.167112-167112, Article 167112
• Main Authors: Seul, Anait, Brasilès, Sandrine, Petitpas, Isabelle, Lurz, Rudi, Campanacci, Valérie, Cambillau, Christian, Weise, Frank, Zairi, Mohamed, Tavares, Paulo, Auzat, Isabelle
• Format: Article
• Language: English
• Subjects: bacteriophage tail; Biochemistry; Biochemistry, Molecular Biology; chaperone; delivery device; Life Sciences; macromolecular assembly; Microbiology and Parasitology; Molecular biology; Quantitative Methods; siphoviruses; tape measure; Virology
• ISSN: 0022-2836; 1089-8638
• DOI: 10.1016/j.jmb.2021.167112

[Display omitted] •Long bacteriophage tails are nanotube devices for delivery of viral DNA to the host cell cytoplasm.•Sequential program of protein interactions leading to assembly of phage SPP1 tail is uncovered.•Tail chaperones are essential to stabilize the TMP structure and for tail tube assembly.•Gp16.1, a highly conserved phage protein, acts during assembly of the tail interface for capsid binding.•SPP1 uses a minimal protein set to build long phage tails. Siphoviruses are main killers of bacteria. They use a long non-contractile tail to recognize the host cell and to deliver the genome from the viral capsid to the bacterial cytoplasm. Here, we define the molecular organization of the Bacillus subtilis bacteriophage SPP1 ~ 6.8 MDa tail and uncover its biogenesis mechanisms. A complex between gp21 and the tail distal protein (Dit) gp19.1 is assembled first to build the tail cap (gp19.1-gp21Nter) connected by a flexible hinge to the tail fiber (gp21Cter). The tip of the gp21Cter fiber is loosely associated to gp22. The cap provides a platform where tail tube proteins (TTPs) initiate polymerization around the tape measure protein gp18 (TMP), a reaction dependent on the non-structural tail assembly chaperones gp17.5 and gp17.5* (TACs). Gp17.5 is essential for stability of gp18 in the cell. Helical polymerization stops at a precise tube length followed by binding of proteins gp16.1 (TCP) and gp17 (THJP) to build the tail interface for attachment to the capsid portal system. This finding uncovers the function of the extensively conserved gp16.1-homologs in assembly of long tails. All SPP1 tail components, apart from gp22, share homology to conserved proteins whose coding genes’ synteny is broadly maintained in siphoviruses. They conceivably represent the minimal essential protein set necessary to build functional long tails. Proteins homologous to SPP1 tail building blocks feature a variety of add-on modules that diversify extensively the tail core structure, expanding its capability to bind host cells and to deliver the viral genome to the bacterial cytoplasm.