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

We 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 still to be determined. Here, we show that phages encoding the major phage nucleus...

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Published in:	Cell reports (Cambridge) Vol. 42; no. 5; p. 112432
Main Authors:	Prichard, Amy, Lee, Jina, Laughlin, Thomas G., Lee, Amber, Thomas, Kyle P., Sy, Annika E., 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 D., Pogliano, Kit, Meyer, Justin, Grose, Julianne H., Villa, Elizabeth, Dutton, Rachel, Pogliano, Joe
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 30-05-2023 Elsevier
Subjects:	Bacteriophages - genetics Bacteriophages - metabolism Chimallin core genome CP: Microbiology cytoskeleton DNA, Viral - genetics DNA, Viral - metabolism Erwinia Erwinia - genetics Erwinia - metabolism Genome, Viral nuclear shell phage phage nucleus phage tubulin PhuZ Phylogeny Erwinia nuclear shell cytoskeleton Chimallin CP: Microbiology PhuZ phage tubulin phage nucleus phage core genome
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Summary:	We 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 still to be determined. Here, we show that phages encoding the major phage nucleus protein chimallin share 72 conserved genes encoded within seven gene blocks. Of these, 21 core genes are unique to nucleus-forming phage, and all but one of these genes encode proteins of unknown function. We propose that these phages comprise a novel viral family we term Chimalliviridae. Fluorescence microscopy and cryoelectron tomography studies of Erwinia phage vB_EamM_RAY confirm that many of the key steps of nucleus-based replication are conserved among diverse chimalliviruses and reveal variations on this replication mechanism. 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. [Display omitted] •Erwinia phage RAY is a nucleus-forming phage•Nucleus-forming phages cluster phylogenetically and share a core genome, including ChmA•We propose that all phage encoding ChmA form a family of nucleus-forming phages Some bacteriophages have been shown to make a nucleus-like structure (the phage nucleus) during their infection cycle. These phages are widespread and infect numerous hosts. Prichard et al. find that these phages cluster together in phylogenetic trees, suggesting a common ancestry of all known nucleus-forming phages.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, A.P., T.S., J.P., and R.D.; data curation, A.P., J.L., and T.G.L.; formal analysis, A.P., J.L., T.G.L., and A.L.; funding acquisition, J.P. and E.V.; investigation, A.P., J.L., T.G.L., A.L., K.P.T., and A.E.S.; methodology, A.P., J.L., and R.D.; project administration, J.P. and R.D.; resources, J.H.G., E.V., J.P., and R.D.; software, J.L.; supervision, J.P. and R.D.; validation, A.P. and J.L.; visualization, A.P., J.L., T.G.L., A.L., and K.P.T.; writing – original draft, A.P., J.L., T.G.L., A.L., K.P.T., A.E.S., T.S., A.A., A.C., M.C., N.C., D.D., I.D., G.D., M.G., K.H., L.H., E.J., A.J., S.K., R.K., A.M., M.N., T.P., G.P., K.S., M.S., A.J.S., S.S., A.S., A.U., A.Z., R.D., and J.P.; writing – review & editing, A.P., J.L., T.G.L., K.D.C., K.P., J.M., J.H.G., E.V., R.D., and J.P.
ISSN:	2211-1247 2211-1247
DOI:	10.1016/j.celrep.2023.112432