Identifying the core genome of the nucleus-forming bacteriophage family and characterization ofErwiniaphage RAY

Author:

Prichard Amy,Lee Jina,Laughlin Thomas G.,Lee Amber,Thomas Kyle P.,Sy Annika,Spencer Tara,Asavavimol Aileen,Cafferata Allison,Cameron Mia,Chiu Nicholas,Davydov Demyan,Desai Isha,Diaz Gabriel,Guereca Melissa,Hearst Kiley,Huang Leyi,Jacobs Emily,Johnson Annika,Kahn Samuel,Koch Ryan,Martinez Adamari,Norquist Meliné,Pau Tyler,Prasad Gino,Saam Katrina,Sandhu Milan,Sarabia Angel Jose,Schumaker Siena,Sonin Aaron,Uyeno Ariya,Zhao Alison,Corbett Kevin,Pogliano Kit,Meyer Justin,Grose Julianne H.,Villa Elizabeth,Dutton Rachel,Pogliano Joe

Abstract

ABSTRACTWe recently discovered that some bacteriophages establish a nucleus-like replication compartment (phage nucleus), but the core genes that define nucleus-based phage replication and their phylogenetic distribution were unknown. By studying phages that encode the major phage nucleus protein chimallin, including previously sequenced yet uncharacterized phages, we discovered that chimallin-encoding phages share a set of 72 highly conserved genes encoded within seven distinct gene blocks. Of these, 21 core genes are unique to this group, and all but one of these unique genes encode proteins of unknown function. We propose that phages with this core genome comprise a novel viral family we term Chimalliviridae. Fluorescence microscopy and cryo-electron tomography studies ofErwiniaphage vB_EamM_RAY confirm that many of the key steps of nucleus-based replication encoded in the core genome are conserved among diverse chimalliviruses, and reveal that non-core components can confer intriguing variations on this replication mechanism. For instance, unlike previously studied nucleus-forming phages, RAY doesn’t degrade the host genome, and its PhuZ homolog appears to form a five-stranded filament with a lumen. This work expands our understanding of phage nucleus and PhuZ spindle diversity and function, providing a roadmap for identifying key mechanisms underlying nucleus-based phage replication.

Publisher

Cold Spring Harbor Laboratory

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