The Opening of the SPP1 Bacteriophage Tail, a Prevalent Mechanism in Gram-positive-infecting Siphophages

Goulet, Adeline; Lai-Kee-Him, Joséphine; Veesler, David; Auzat, Isabelle; Robin, Gautier; Shepherd, Dale A.; Ashcroft, Alison E.; Richard, Eric; Lichière, Julie; Tavares, Paulo; Cambillau, Christian; Bron, Patrick

doi:10.1074/jbc.m111.243360

Cited by 42 publications

(68 citation statements)

References 44 publications

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“…S1 B, D, and F) to YueB780 leads to disassembly of the tip, providing a visual signature of the interaction (yellow arrows in Fig. S1 C, E, and G) (17,18). This interaction correlates with the release of DNA from the HTI of most connector-tail complexes, as monitored by visualization of DNA after adsorption to mica (Fig.…”

Section: Resultsmentioning

confidence: 99%

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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Section: Resultsmentioning

confidence: 99%

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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“…4B). The tail tube delineates a 42-Å-wide central channel that is continuous with the connector and baseplate channels to form the genome ejection pathway (5,11,12,27,30,31) (Fig. 4C and D).…”

Section: Resultsmentioning

confidence: 99%

Visualizing a Complete Siphoviridae Member by Single-Particle Electron Microscopy: the Structure of Lactococcal Phage TP901-1

Bebeacua

Lai

Vegge

et al. 2013

J Virol

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c Tailed phages are genome delivery machines exhibiting unequaled efficiency acquired over more than 3 billion years of evolution. Siphophages from the P335 and 936 families infect the Gram-positive bacterium Lactococcus lactis using receptor-binding proteins anchored to the host adsorption apparatus (baseplate). Crystallographic and electron microscopy (EM) studies have shed light on the distinct adsorption strategies used by phages of these two families, suggesting that they might also rely on different infection mechanisms. Here, we report electron microscopy reconstructions of the whole phage TP901-1 (P335 species) and propose a composite EM model of this gigantic molecular machine. Our results suggest conservation of structural proteins among tailed phages and add to the growing body of evidence pointing to a common evolutionary origin for these virions. Finally, we propose that host adsorption apparatus architectures have evolved in correlation with the nature of the receptors used during infection.

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“…Finally, a 34-Å-wide central channel is present in the center of the tail tube, aligned with the connector and baseplate channels, forming the dsDNA genome ejection pathway (17,(47)(48)(49)(50)(51) (Fig. 5G).…”

Section: Sequence Analysismentioning

confidence: 99%

Cryo-Electron Microscopy Structure of Lactococcal Siphophage 1358 Virion

Spinelli

Bebeacua

Orlov

et al. 2014

J Virol

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Lactococcus lactis, a Gram؉ lactic acid-producing bacterium used for the manufacture of several fermented dairy products, is subject to infection by diverse virulent tailed phages, leading to industrial fermentation failures. This constant viral risk has led to a sustained interest in the study of their biology, diversity, and evolution. Lactococcal phages now constitute a wide ensemble of at least 10 distinct genotypes within the Caudovirales order, many of them belonging to the Siphoviridae family. Lactococcal siphophage 1358, currently the only member of its group, displays a noticeably high genomic similarity to some Listeria phages as well as a host range limited to a few L. lactis strains. These genomic and functional characteristics stimulated our interest in this phage. Here, we report the cryo-electron microscopy structure of the complete 1358 virion. Phage 1358 exhibits noteworthy features, such as a capsid with dextro handedness and protruding decorations on its capsid and tail. Observations of the baseplate of virion particles revealed at least two conformations, a closed and an open, activated form. Functional assays uncovered that the adsorption of phage 1358 to its host is Ca 2؉ independent, but this cation is necessary to complete its lytic cycle. Taken together, our results provide the complete structural picture of a unique lactococcal phage and expand our knowledge on the complex baseplate of phages of the Siphoviridae family. IMPORTANCE Phages of Lactococcus lactis are investigated mainly because they are sources of milk fermentation failures in the dairy industry.Despite the availability of several antiphage measures, new phages keep emerging in this ecosystem. In this study, we provide the cryo-electron microscopy reconstruction of a unique lactococcal phage that possesses genomic similarity to particular Listeria phages and has a host range restricted to only a minority of L. lactis strains. The capsid of phage 1358 displays the almost unique characteristic of being dextro handed. Its capsid and tail exhibit decorations that we assigned to nonspecific sugar binding modules. We observed the baseplate of 1358 in two conformations, a closed and an open form. We also found that the adsorption to its host, but not infection, is Ca 2؉ independent. Overall, this study advances our understanding of the adhesion mechanisms of siphophages.

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The Opening of the SPP1 Bacteriophage Tail, a Prevalent Mechanism in Gram-positive-infecting Siphophages

Cited by 42 publications

References 44 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

Visualizing a Complete Siphoviridae Member by Single-Particle Electron Microscopy: the Structure of Lactococcal Phage TP901-1

Cryo-Electron Microscopy Structure of Lactococcal Siphophage 1358 Virion

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