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A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to posit...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4244570/ https://www.ncbi.nlm.nih.gov/pubmed/25429514 http://dx.doi.org/10.7554/eLife.03197 |
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author | Erb, Marcella L Kraemer, James A Coker, Joanna K C Chaikeeratisak, Vorrapon Nonejuie, Poochit Agard, David A Pogliano, Joe |
author_facet | Erb, Marcella L Kraemer, James A Coker, Joanna K C Chaikeeratisak, Vorrapon Nonejuie, Poochit Agard, David A Pogliano, Joe |
author_sort | Erb, Marcella L |
collection | PubMed |
description | Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to position DNA at mid-cell, without which infectivity is compromised. Here, we show that PhuZ filaments, like microtubules, stochastically switch from growing in a distinctly polar manner to catastrophic depolymerization (dynamic instability) both in vitro and in vivo. One end of each PhuZ filament is stably anchored near the cell pole to form a spindle-like array that orients the growing ends toward the phage nucleoid so as to position it near mid-cell. Our results demonstrate how a bacteriophage can harness the properties of a tubulin-like cytoskeleton for efficient propagation. This represents the first identification of a prokaryotic tubulin with the dynamic instability of microtubules and the ability to form a simplified bipolar spindle. DOI: http://dx.doi.org/10.7554/eLife.03197.001 |
format | Online Article Text |
id | pubmed-4244570 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-42445702014-12-18 A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells Erb, Marcella L Kraemer, James A Coker, Joanna K C Chaikeeratisak, Vorrapon Nonejuie, Poochit Agard, David A Pogliano, Joe eLife Cell Biology Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to position DNA at mid-cell, without which infectivity is compromised. Here, we show that PhuZ filaments, like microtubules, stochastically switch from growing in a distinctly polar manner to catastrophic depolymerization (dynamic instability) both in vitro and in vivo. One end of each PhuZ filament is stably anchored near the cell pole to form a spindle-like array that orients the growing ends toward the phage nucleoid so as to position it near mid-cell. Our results demonstrate how a bacteriophage can harness the properties of a tubulin-like cytoskeleton for efficient propagation. This represents the first identification of a prokaryotic tubulin with the dynamic instability of microtubules and the ability to form a simplified bipolar spindle. DOI: http://dx.doi.org/10.7554/eLife.03197.001 eLife Sciences Publications, Ltd 2014-11-27 /pmc/articles/PMC4244570/ /pubmed/25429514 http://dx.doi.org/10.7554/eLife.03197 Text en Copyright © 2014, Erb et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Cell Biology Erb, Marcella L Kraemer, James A Coker, Joanna K C Chaikeeratisak, Vorrapon Nonejuie, Poochit Agard, David A Pogliano, Joe A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title | A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title_full | A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title_fullStr | A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title_full_unstemmed | A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title_short | A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells |
title_sort | bacteriophage tubulin harnesses dynamic instability to center dna in infected cells |
topic | Cell Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4244570/ https://www.ncbi.nlm.nih.gov/pubmed/25429514 http://dx.doi.org/10.7554/eLife.03197 |
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