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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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 |
work_keys_str_mv |
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