Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating

Lhuillier, Sophie; Gallopin, Matthieu; Gilquin, Bernard; Brasilès, Sandrine; Lancelot, Nathalie; Letellier, Guillaume; Gilles, M; Dethan, G; Orlova, Elena V.; Couprie, Joël; Tavares, Paulo; Zinn‐Justin, Sophie

doi:10.1073/pnas.0812407106

Cited by 112 publications

(152 citation statements)

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“…S5A). This rearrangement of gp15 during virus assembly is less dramatic than previously proposed (13). GP15 contacts gp6 via its loop α1-α2 (brown arrow in Fig.…”

Section: Resultsmentioning

confidence: 64%

“…The alternate distribution of subunits along the structure's height provides a mechanism for assembly in which oligomerization of one protein creates the interface for stable binding of the following interaction partner. This organization ensures orderly assembly and prevents premature interaction between components of the HTI that are monomeric before assembly (gp15, gp16, and gp17) (13)(14)(15) and that do not interact with each other in solution (gp6, gp15, and gp16) (13).…”

Section: Resultsmentioning

confidence: 99%

“…Termination of DNA packaging is coordinated with disassembly of the motor and binding of gp15 subunits (11.6 kDa) to gp6, extending the portal channel that is closed underneath by the gp16 protein (12.5 kDa) (Fig. S1A) (13). The assembled complex represents the 180-Å-high connector that consists of three stacked cyclical homo-oligomers, each composed of 12 subunits of the portal protein gp6, of the adaptor gp15, and of the stopper gp16 (4,13).…”

mentioning

confidence: 99%

“…S1A) (13). The assembled complex represents the 180-Å-high connector that consists of three stacked cyclical homo-oligomers, each composed of 12 subunits of the portal protein gp6, of the adaptor gp15, and of the stopper gp16 (4,13). Gp16 operates as a docking platform for the SPP1 preassembled tail tapered by the tail-to-head joining protein gp17 (15 kDa) (14,15).…”

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confidence: 99%

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Structural rearrangements in the phage head-to-tail interface during assembly and infection

Chaban

Lurz

Brasilès

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Many icosahedral viruses use a specialized portal vertex to control genome encapsidation and release from the viral capsid. In tailed bacteriophages, the portal system is connected to a tail structure that provides the pipeline for genome delivery to the host cell. We report the first, to our knowledge, subnanometer structures of the complete portal-phage tail interface that mimic the states before and after DNA release during phage infection. They uncover structural rearrangements associated with intimate protein-DNA interactions. The portal protein gp6 of bacteriophage SPP1 undergoes a concerted reorganization of the structural elements of its central channel during interaction with DNA. A network of protein-protein interactions primes consecutive binding of proteins gp15 and gp16 to extend and close the channel. This critical step that prevents genome leakage from the capsid is achieved by a previously unidentified allosteric mechanism: gp16 binding to two different regions of gp15 drives correct positioning and folding of an inner gp16 loop to interact with equivalent loops of the other gp16 subunits. Together, these loops build a plug that closes the channel. Gp16 then fastens the tail to yield the infectious virion. The gatekeeper system opens for viral genome exit at the beginning of infection but recloses afterward, suggesting a molecular diaphragm-like mechanism to control DNA efflux. The mechanisms described here, controlling the essential steps of phage genome movements during virus assembly and infection, are likely to be conserved among long-tailed phages, the largest group of viruses in the Biosphere.DNA gatekeeper | viral infection | bacteriophage | allosteric mechanism | hybrid methods

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“…S5A). This rearrangement of gp15 during virus assembly is less dramatic than previously proposed (13). GP15 contacts gp6 via its loop α1-α2 (brown arrow in Fig.…”

Section: Resultsmentioning

confidence: 64%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Structural rearrangements in the phage head-to-tail interface during assembly and infection

Chaban

Lurz

Brasilès

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…5E and F). Dodecameric models of gp15 and gp16 were those used for fitting in the SPP1 map in the work of Lhuillier et al (44).…”

Section: Genome Characteristics Of Mycobacteriophagementioning

confidence: 99%

The First Structure of a Mycobacteriophage, the Mycobacterium abscessus subsp. bolletii Phage Araucaria

Sassi

Bebeacua

Drancourt

et al. 2013

J Virol

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The unique characteristics of the waxy mycobacterial cell wall raise questions about specific structural features of their bacteriophages. No structure of any mycobacteriophage is available, although ϳ3,500 have been described to date. To fill this gap, we embarked in a genomic and structural study of a bacteriophage from Mycobacterium abscessus subsp. bolletii, a member of the Mycobacterium abscessus group. This opportunistic pathogen is responsible for respiratory tract infections in patients with lung disorders, particularly cystic fibrosis. M. abscessus subsp. bolletii was isolated from respiratory tract specimens, and bacteriophages were observed in the cultures. We report here the genome annotation and characterization of the M. abscessus subsp. bolletii prophage Araucaria, as well as the first single-particle electron microscopy reconstruction of the whole virion. Araucaria belongs to Siphoviridae and possesses a 64-kb genome containing 89 open reading frames (ORFs), among which 27 could be annotated with certainty. Although its capsid and connector share close similarity with those of several phages from Gram-negative (Gram ؊ ) or Gram ؉ bacteria, its most distinctive characteristic is the helical tail decorated by radial spikes, possibly host adhesion devices, according to which the phage name was chosen. Its host adsorption device, at the tail tip, assembles features observed in phages binding to protein receptors, such as phage SPP1. All together, these results suggest that Araucaria may infect its mycobacterial host using a mechanism involving adhesion to cell wall saccharides and protein, a feature that remains to be further explored.

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Bacteriophages: Structure

Cuervo

Carrascosa

2012

Encyclopedia of Life Sciences

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Bacterial viruses, or bacteriophages, are ubiquitous organisms spanning very different ecological niches. Although genome comparison fails to show extensive relationship among bacteriophages, recent structural studies reveal a high degree of similarities. Most bacteriophages present an icosahedral proteinaceous head, which contains the nucleic acid, either deoxyribonucleic acid (DNA) or ribonucleic acid (RNA) . Exceptions to this rule are few cases where a lipid envelope forms part of the head, and those other cases where the head presents a filamentous geometry. The way bacteriophages infect the host cell is the basis of a main difference among them: one group (Caudovirales) has a specialised structure (the tail) that is responsible for the recognition of the host cell and the viral genome delivery, whereas those bacteriophages without tail present a variety of infecting strategies. In this study we will deal with the main common characteristics of bacteriophage heads and tails supporting their common evolutionary origin. Key Concepts: Bacteriophages share extended structural and functional similarities. Bacteriophages are excellent examples of optimisation of genetic information to carry out complex functions. Most bacteriophages enclose their nucleic acid in a protein container (built by multiple copies of one (or a few) proteins), and in a few cases they may include lipid envelopes. The most conserved geometry in bacteriophage heads is icosahedral. Double stranded DNA icosahedral bacteriophages follow a common assembly pathway. The Caudovirales group (bacteriophages with icosahedral heads, dsDNA and a tail) are the most abundant virus type. The packaging of dsDNA inside Caudovirales requires energy conversion (ATP hydrolysis) into mechanical translocation, and it is carried out by a dedicated viral machinery. The maturation of icosahedral proheads into viral heads involves drastic reorganisations of the capsid components leading to more stable particles. The tail of Caudovirales is a sophisticated machinery involved in cell recognition and nucleic acids delivery. There are three main architectural designs of bacteriophage tails, each one adapting to different host interaction strategies.

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Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating

Cited by 112 publications

References 39 publications

Structural rearrangements in the phage head-to-tail interface during assembly and infection

Structural rearrangements in the phage head-to-tail interface during assembly and infection

The First Structure of a Mycobacteriophage, the Mycobacterium abscessus subsp. bolletii Phage Araucaria

Bacteriophages: Structure

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