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...

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Main Authors: Marcella L Erb, James A Kraemer, Joanna K C Coker, Vorrapon Chaikeeratisak, Poochit Nonejuie, David A Agard, Joe Pogliano
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/03197
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spelling doaj-19b8e4b5d4864b308caf5207a33ad3af2021-05-04T23:33:25ZengeLife Sciences Publications LtdeLife2050-084X2014-11-01310.7554/eLife.03197A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cellsMarcella L Erb0James A Kraemer1Joanna K C Coker2Vorrapon Chaikeeratisak3Poochit Nonejuie4David A Agard5Joe Pogliano6Division of Biological Sciences, University of California, San Diego, La Jolla, United StatesDepartment of Biochemistry and Biophysics, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDivision of Biological Sciences, University of California, San Diego, La Jolla, United StatesDivision of Biological Sciences, University of California, San Diego, La Jolla, United StatesDivision of Biological Sciences, University of California, San Diego, La Jolla, United StatesDepartment of Biochemistry and Biophysics, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDivision of Biological Sciences, University of California, San Diego, La Jolla, United StatesDynamic 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.https://elifesciences.org/articles/03197tubulincytoskeletondynamic instabilityspindlepseudomonasbacteriophage
collection DOAJ
language English
format Article
sources DOAJ
author Marcella L Erb
James A Kraemer
Joanna K C Coker
Vorrapon Chaikeeratisak
Poochit Nonejuie
David A Agard
Joe Pogliano
spellingShingle Marcella L Erb
James A Kraemer
Joanna K C Coker
Vorrapon Chaikeeratisak
Poochit Nonejuie
David A Agard
Joe Pogliano
A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
eLife
tubulin
cytoskeleton
dynamic instability
spindle
pseudomonas
bacteriophage
author_facet Marcella L Erb
James A Kraemer
Joanna K C Coker
Vorrapon Chaikeeratisak
Poochit Nonejuie
David A Agard
Joe Pogliano
author_sort Marcella L Erb
title 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_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_sort bacteriophage tubulin harnesses dynamic instability to center dna in infected cells
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2014-11-01
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.
topic tubulin
cytoskeleton
dynamic instability
spindle
pseudomonas
bacteriophage
url https://elifesciences.org/articles/03197
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