Cargando…

The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages

Bacteriophages and their bacterial hosts are ancient organisms that have been co-evolving for billions of years. Some jumbo phages, those with a genome size larger than 200 kilobases, have recently been discovered to establish complex subcellular organization during replication. Here, we review our...

Descripción completa

Detalles Bibliográficos
Autores principales: Chaikeeratisak, Vorrapon, Birkholz, Erica A., Pogliano, Joe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314001/
https://www.ncbi.nlm.nih.gov/pubmed/34326818
http://dx.doi.org/10.3389/fmicb.2021.641317
_version_ 1783729460140310528
author Chaikeeratisak, Vorrapon
Birkholz, Erica A.
Pogliano, Joe
author_facet Chaikeeratisak, Vorrapon
Birkholz, Erica A.
Pogliano, Joe
author_sort Chaikeeratisak, Vorrapon
collection PubMed
description Bacteriophages and their bacterial hosts are ancient organisms that have been co-evolving for billions of years. Some jumbo phages, those with a genome size larger than 200 kilobases, have recently been discovered to establish complex subcellular organization during replication. Here, we review our current understanding of jumbo phages that form a nucleus-like structure, or “Phage Nucleus,” during replication. The phage nucleus is made of a proteinaceous shell that surrounds replicating phage DNA and imparts a unique subcellular organization that is temporally and spatially controlled within bacterial host cells by a phage-encoded tubulin (PhuZ)-based spindle. This subcellular architecture serves as a replication factory for jumbo Pseudomonas phages and provides a selective advantage when these replicate in some host strains. Throughout the lytic cycle, the phage nucleus compartmentalizes proteins according to function and protects the phage genome from host defense mechanisms. Early during infection, the PhuZ spindle positions the newly formed phage nucleus at midcell and, later in the infection cycle, the spindle rotates the nucleus while delivering capsids and distributing them uniformly on the nuclear surface, where they dock for DNA packaging. During the co-infection of two different nucleus-forming jumbo phages in a bacterial cell, the phage nucleus establishes Subcellular Genetic Isolation that limits the potential for viral genetic exchange by physically separating co-infection genomes, and the PhuZ spindle causes Virogenesis Incompatibility, whereby interacting components from two diverging phages negatively affect phage reproduction. Thus, the phage nucleus and PhuZ spindle are defining cell biological structures that serve roles in both the life cycle of nucleus-forming jumbo phages and phage speciation.
format Online
Article
Text
id pubmed-8314001
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-83140012021-07-28 The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages Chaikeeratisak, Vorrapon Birkholz, Erica A. Pogliano, Joe Front Microbiol Microbiology Bacteriophages and their bacterial hosts are ancient organisms that have been co-evolving for billions of years. Some jumbo phages, those with a genome size larger than 200 kilobases, have recently been discovered to establish complex subcellular organization during replication. Here, we review our current understanding of jumbo phages that form a nucleus-like structure, or “Phage Nucleus,” during replication. The phage nucleus is made of a proteinaceous shell that surrounds replicating phage DNA and imparts a unique subcellular organization that is temporally and spatially controlled within bacterial host cells by a phage-encoded tubulin (PhuZ)-based spindle. This subcellular architecture serves as a replication factory for jumbo Pseudomonas phages and provides a selective advantage when these replicate in some host strains. Throughout the lytic cycle, the phage nucleus compartmentalizes proteins according to function and protects the phage genome from host defense mechanisms. Early during infection, the PhuZ spindle positions the newly formed phage nucleus at midcell and, later in the infection cycle, the spindle rotates the nucleus while delivering capsids and distributing them uniformly on the nuclear surface, where they dock for DNA packaging. During the co-infection of two different nucleus-forming jumbo phages in a bacterial cell, the phage nucleus establishes Subcellular Genetic Isolation that limits the potential for viral genetic exchange by physically separating co-infection genomes, and the PhuZ spindle causes Virogenesis Incompatibility, whereby interacting components from two diverging phages negatively affect phage reproduction. Thus, the phage nucleus and PhuZ spindle are defining cell biological structures that serve roles in both the life cycle of nucleus-forming jumbo phages and phage speciation. Frontiers Media S.A. 2021-07-13 /pmc/articles/PMC8314001/ /pubmed/34326818 http://dx.doi.org/10.3389/fmicb.2021.641317 Text en Copyright © 2021 Chaikeeratisak, Birkholz and Pogliano. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Chaikeeratisak, Vorrapon
Birkholz, Erica A.
Pogliano, Joe
The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title_full The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title_fullStr The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title_full_unstemmed The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title_short The Phage Nucleus and PhuZ Spindle: Defining Features of the Subcellular Organization and Speciation of Nucleus-Forming Jumbo Phages
title_sort phage nucleus and phuz spindle: defining features of the subcellular organization and speciation of nucleus-forming jumbo phages
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314001/
https://www.ncbi.nlm.nih.gov/pubmed/34326818
http://dx.doi.org/10.3389/fmicb.2021.641317
work_keys_str_mv AT chaikeeratisakvorrapon thephagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages
AT birkholzericaa thephagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages
AT poglianojoe thephagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages
AT chaikeeratisakvorrapon phagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages
AT birkholzericaa phagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages
AT poglianojoe phagenucleusandphuzspindledefiningfeaturesofthesubcellularorganizationandspeciationofnucleusformingjumbophages