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Architecture and Self-assembly of the Jumbo Bacteriophage Nuclear Shell

Abstract

Bacteria encode myriad defences that target the genomes of infecting bacteriophage, including restriction-modification and CRISPR-Cas systems. In response, one family of large bacteriophages uses a nucleus-like compartment to protect its replicating genomes by excluding host defence factors. 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.

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References
1.
Koonin E, Makarova K, Wolf Y . Evolutionary Genomics of Defense Systems in Archaea and Bacteria. Annu Rev Microbiol. 2017; 71:233-261. PMC: 5898197. DOI: 10.1146/annurev-micro-090816-093830. View

2.
Chaikeeratisak V, Nguyen K, Khanna K, Brilot A, Erb M, Coker J . Assembly of a nucleus-like structure during viral replication in bacteria. Science. 2017; 355(6321):194-197. PMC: 6028185. DOI: 10.1126/science.aal2130. View

3.
Mendoza S, Nieweglowska E, Govindarajan S, Leon L, Berry J, Tiwari A . A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases. Nature. 2019; 577(7789):244-248. PMC: 6949375. DOI: 10.1038/s41586-019-1786-y. View

4.
Malone L, Warring S, Jackson S, Warnecke C, Gardner P, Gumy L . A jumbo phage that forms a nucleus-like structure evades CRISPR-Cas DNA targeting but is vulnerable to type III RNA-based immunity. Nat Microbiol. 2019; 5(1):48-55. DOI: 10.1038/s41564-019-0612-5. View

5.
Rostol J, Marraffini L . (Ph)ighting Phages: How Bacteria Resist Their Parasites. Cell Host Microbe. 2019; 25(2):184-194. PMC: 6383810. DOI: 10.1016/j.chom.2019.01.009. View