A Common Evolutionary Origin for Tailed-Bacteriophage Functional Modules and Bacterial Machineries

Veesler, David; Cambillau, Christian

doi:10.1128/mmbr.00014-11

Cited by 249 publications

(270 citation statements)

References 92 publications

(140 reference statements)

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“…Furthermore, the receptor-binding protein trimers of phages p2 and 1358 point toward the bacteriophage head in the native state and require a 200°rotation to orient themselves toward the putative bacterial cell wall (24,25). These structural and functional similarities reinforce the previously suggested common ancestry of the Siphoviridae and Myoviridae families (26).…”

Section: Significancesupporting

confidence: 68%

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Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Nováček

Šiborová

Benešík

et al. 2016

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

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Bacteriophages from the family Myoviridae use double-layered contractile tails to infect bacteria. Contraction of the tail sheath enables the tail tube to penetrate through the bacterial cell wall and serve as a channel for the transport of the phage genome into the cytoplasm. However, the mechanisms controlling the tail contraction and genome release of phages with “double-layered” baseplates were unknown. We used cryo-electron microscopy to show that the binding of the Twort-like phage phi812 to the Staphylococcus aureus cell wall requires a 210° rotation of the heterohexameric receptor-binding and tripod protein complexes within its baseplate about an axis perpendicular to the sixfold axis of the tail. This rotation reorients the receptor-binding proteins to point away from the phage head, and also results in disruption of the interaction of the tripod proteins with the tail sheath, hence triggering its contraction. However, the tail sheath contraction of Myoviridae phages is not sufficient to induce genome ejection. We show that the end of the phi812 double-stranded DNA genome is bound to one protein subunit from a connector complex that also forms an interface between the phage head and tail. The tail sheath contraction induces conformational changes of the neck and connector that result in disruption of the DNA binding. The genome penetrates into the neck, but is stopped at a bottleneck before the tail tube. A subsequent structural change of the tail tube induced by its interaction with the S. aureus cell is required for the genome’s release.

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Section: Significancesupporting

confidence: 68%

“…Bacteriophage tails are attached to heads through a connector complex positioned at a special vertex in which a portal complex replaces the pentamer of major capsid proteins (26). The phi812 connector contains a dome-shaped "gateway" density interacting with the portal complex (Figs.…”

Section: Significancementioning

confidence: 99%

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Nováček

Šiborová

Benešík

et al. 2016

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

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“…5B and C). The large number of MCP structures reported to date has established the conservation of the HK97 MCP fold (so-called "Johnson fold") among tailed phages, herpesviruses, and some archaeal viruses (36)(37)(38)(39). The HK97 MCP hexamers and pentamers could be fitted readily in the capsid EM structure (Fig.…”

Section: Genome Characteristics Of Mycobacteriophagementioning

confidence: 96%

“…The portal, a dodecameric protein, discloses a conserved fold in tailed phages and herpesviruses (14,36). It is involved in DNA packaging during assembly and in DNA release when phage infection occurs.…”

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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“…Numerous major bacterial innovations stem from the co-option of viral hardware including gene transfer agents (virus-like particles that transfer bacterial DNA only) [50] and type VI secretion systems (phage-derived syringes to inject or puncture neighboring cells). [51] Deactivated prophages can also act as regulatory switches -a process called "active lysogeny." [52] Here, prophages sit within the coding region of the gene disrupting gene function.…”

Section: Temperate Phages As Sources Of Genetic Variation For Evolumentioning

confidence: 99%

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

2017

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Infection by a temperate phage can lead to death of the bacterial cell, but sometimes these phages integrate into the bacterial chromosome, offering the potential for a more long-lasting relationship to be established. Here we define three major ecological and evolutionary benefits of temperate phage for bacteria: as agents of horizontal gene transfer (HGT), as sources of genetic variation for evolutionary innovation, and as weapons of bacterial competition. We suggest that a coevolutionary perspective is required to understand the roles of temperate phages in bacterial populations.

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A Common Evolutionary Origin for Tailed-Bacteriophage Functional Modules and Bacterial Machineries

Cited by 249 publications

References 92 publications

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

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

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

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