A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in <i>E. coli</i>

Birkholz, Erica A.; Laughlin, Thomas G.; Suslov, Sergey; Armbruster, Emily; Lee, Jina; Wittmann, Johannes; Corbett, K.D.; Villa, Elizabeth; Pogliano, Joe

doi:10.1101/2021.10.25.465362

Cited by 9 publications

(12 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Therefore, it seems likely that these assemblages are not essential for these phages to reproduce. However, we have recently shown that Escherichia coli jumbo phage Goslar also forms a nucleus and large phage bouquets late during infection, demonstrating that this phenomenon is conserved in a distantly related jumbo phage (41). We do not observe intact bouquets after cell lysis by fluorescence microscopy, suggesting that they do not survive the forceful lysis of the host cell.…”

Section: Resultsmentioning

confidence: 53%

Subcellular organization of viral particles during maturation of nucleus-forming jumbo phage

et al. 2022

Self Cite

View full text Add to dashboard Cite

Many eukaryotic viruses assemble mature particles within distinct subcellular compartments, but bacteriophages are generally assumed to assemble randomly throughout the host cell cytoplasm. Here, we show that viral particles of Pseudomonas nucleus-forming jumbo phage PhiPA3 assemble into a unique structure inside cells we term phage bouquets. We show that after capsids complete DNA packaging at the surface of the phage nucleus, tails assemble and attach to capsids, and these particles accumulate over time in a spherical pattern, with tails oriented inward and the heads outward to form bouquets at specific subcellular locations. Bouquets localize at the same fixed distance from the phage nucleus even when it is mispositioned, suggesting an active mechanism for positioning. These results mark the discovery of a pathway for organizing mature viral particles inside bacteria and demonstrate that nucleus-forming jumbo phages, like most eukaryotic viruses, are highly spatially organized during all stages of their lytic cycle.

show abstract

Section: Resultsmentioning

confidence: 53%

Subcellular organization of viral particles during maturation of nucleus-forming jumbo phage

et al. 2022

Self Cite

View full text Add to dashboard Cite

show abstract

“…We recently discovered that the E. coli bacteriophage Goslar assembles a nuclear shell morphologically similar to those observed in the Pseudomonas phage 201φ2-1, φPA3, and φKZ (16). Goslar encodes a divergent homolog of 201φ2-1 chimallin (gp189), with 19.3% overall sequence identity between the two proteins ( Fig.…”

Section: Resultsmentioning

confidence: 76%

Architecture and self-assembly of the jumbo bacteriophage nuclear shell

Laughlin¹,

Deep

Prichard³

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

Bacteria encode myriad defenses that target the genomes of infecting bacteriophage, including restriction-modification and CRISPR/Cas systems. In response, one family of large bacteriophage employs a nucleus-like compartment to protect their replicating genomes by excluding host defense factors. However, the principle composition and structure of this compartment remain unknown. Here, we find that the bacteriophage nuclear shell assembles primarily from one protein, termed chimallin. Combining cryo-electron tomography of nuclear shells in bacteriophage-infected cells and cryo-electron microscopy of a minimal chimallin compartment in vitro, we show that chimallin cooperatively self-assembles as a flexible sheet into closed micron-scale compartments. The architecture and assembly dynamics of the chimallin shell suggest mechanisms for its nucleation and growth, and its role as a scaffold for phage-encoded factors mediating macromolecular transport, cytoskeletal interactions, and viral maturation.

show abstract

“…The E. coli jumbo bacteriophage Goslar (237 kb genome) assembles a nuclear shell morphologically similar to those observed in the Pseudomonas phages 201phi2-1, PhiPA3 and PhiKZ 15 . Goslar encodes a divergent homologue of 201phi2-1 chimallin (gp189, 631 amino acids), with 19.3% overall sequence identity between the two proteins (Fig.…”

Section: Nuclear Shell Architecture Is Conservedmentioning

confidence: 64%

Architecture and self-assembly of the jumbo bacteriophage nuclear shell

Laughlin

Deep

Prichard

et al. 2022

Nature

Self Cite

View full text Add to dashboard Cite

Bacteria encode myriad defences that target the genomes of infecting bacteriophage, including restriction–modification and CRISPR–Cas systems1. In response, one family of large bacteriophages uses a nucleus-like compartment to protect its replicating genomes by excluding host defence factors2–4. However, the principal composition and structure of this compartment remain unknown. Here we find that the bacteriophage nuclear shell assembles primarily from one protein, which we name chimallin (ChmA). Combining cryo-electron tomography of nuclear shells in bacteriophage-infected cells and cryo-electron microscopy of a minimal chimallin compartment in vitro, we show that chimallin self-assembles as a flexible sheet into closed micrometre-scale compartments. The architecture and assembly dynamics of the chimallin shell suggest mechanisms for its nucleation and growth, and its role as a scaffold for phage-encoded factors mediating macromolecular transport, cytoskeletal interactions, and viral maturation.

show abstract

A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli

Cited by 9 publications

References 44 publications

Subcellular organization of viral particles during maturation of nucleus-forming jumbo phage

Subcellular organization of viral particles during maturation of nucleus-forming jumbo phage

Architecture and self-assembly of the jumbo bacteriophage nuclear shell

Architecture and self-assembly of the jumbo bacteriophage nuclear shell

Contact Info

Product

Resources

About