Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation
(2017) In Proceedings of the National Academy of Sciences of the United States of America 114(30). p.6176-6183- Abstract
During sporulation, the filamentous bacteria Streptomyces undergo a massive cell division event in which the synthesis of ladders of sporulation septa convert multigenomic hyphae into chains of unigenomic spores. This process requires cytokinetic Z-rings formed by the bacterial tubulin homolog FtsZ, and the stabilization of the newly formed Z-rings is crucial for completion of septum synthesis. Here we show that two dynamin-like proteins, DynA and DynB, play critical roles in this process. Dynamins are a family of large, multidomain GTPases involved in key cellular processes in eukaryotes, including vesicle trafficking and organelle division. Many bacterial genomes encode dynamin-like proteins, but the biological function of these... (More)
During sporulation, the filamentous bacteria Streptomyces undergo a massive cell division event in which the synthesis of ladders of sporulation septa convert multigenomic hyphae into chains of unigenomic spores. This process requires cytokinetic Z-rings formed by the bacterial tubulin homolog FtsZ, and the stabilization of the newly formed Z-rings is crucial for completion of septum synthesis. Here we show that two dynamin-like proteins, DynA and DynB, play critical roles in this process. Dynamins are a family of large, multidomain GTPases involved in key cellular processes in eukaryotes, including vesicle trafficking and organelle division. Many bacterial genomes encode dynamin-like proteins, but the biological function of these proteins has remained largely enigmatic. Using a cell biological approach, we show that the two Streptomyces dynamins specifically localize to sporulation septa in an FtsZ-dependent manner. Moreover, dynamin mutants have a cell division defect due to the decreased stability of sporulation-specific Z-rings, as demonstrated by kymographs derived from time-lapse images of FtsZ ladder formation. This defect causes the premature disassembly of individual Z-rings, leading to the frequent abortion of septum synthesis, which in turn results in the production of long spore-like compartments with multiple chromosomes. Two-hybrid analysis revealed that the dynamins are part of the cell division machinery and that they mediate their effects on Z-ring stability during developmentally controlled cell division via a network of protein–protein interactions involving DynA, DynB, FtsZ, SepF, SepF2, and the FtsZ-positioning protein SsgB.
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- author
- Schlimpert, Susan ; Wasserstrom, Sebastian LU ; Chandra, Govind ; Bibb, Maureen J. ; Findlay, Kim C. ; Flärdh, Klas LU and Buttner, Mark J.
- organization
- publishing date
- 2017-07-25
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Bacterial dynamins, Cell division, FtsZ, Sporulation, Streptomyces
- in
- Proceedings of the National Academy of Sciences of the United States of America
- volume
- 114
- issue
- 30
- pages
- 6176 - 6183
- publisher
- National Academy of Sciences
- external identifiers
-
- pmid:28687675
- wos:000406189900020
- scopus:85025670503
- ISSN
- 0027-8424
- DOI
- 10.1073/pnas.1704612114
- language
- English
- LU publication?
- yes
- id
- 1e971738-dc75-4b75-9313-03978a9abc8b
- date added to LUP
- 2017-08-02 07:42:12
- date last changed
- 2025-01-07 18:07:54
@article{1e971738-dc75-4b75-9313-03978a9abc8b,
abstract = {{<p>During sporulation, the filamentous bacteria Streptomyces undergo a massive cell division event in which the synthesis of ladders of sporulation septa convert multigenomic hyphae into chains of unigenomic spores. This process requires cytokinetic Z-rings formed by the bacterial tubulin homolog FtsZ, and the stabilization of the newly formed Z-rings is crucial for completion of septum synthesis. Here we show that two dynamin-like proteins, DynA and DynB, play critical roles in this process. Dynamins are a family of large, multidomain GTPases involved in key cellular processes in eukaryotes, including vesicle trafficking and organelle division. Many bacterial genomes encode dynamin-like proteins, but the biological function of these proteins has remained largely enigmatic. Using a cell biological approach, we show that the two Streptomyces dynamins specifically localize to sporulation septa in an FtsZ-dependent manner. Moreover, dynamin mutants have a cell division defect due to the decreased stability of sporulation-specific Z-rings, as demonstrated by kymographs derived from time-lapse images of FtsZ ladder formation. This defect causes the premature disassembly of individual Z-rings, leading to the frequent abortion of septum synthesis, which in turn results in the production of long spore-like compartments with multiple chromosomes. Two-hybrid analysis revealed that the dynamins are part of the cell division machinery and that they mediate their effects on Z-ring stability during developmentally controlled cell division via a network of protein–protein interactions involving DynA, DynB, FtsZ, SepF, SepF2, and the FtsZ-positioning protein SsgB.</p>}},
author = {{Schlimpert, Susan and Wasserstrom, Sebastian and Chandra, Govind and Bibb, Maureen J. and Findlay, Kim C. and Flärdh, Klas and Buttner, Mark J.}},
issn = {{0027-8424}},
keywords = {{Bacterial dynamins; Cell division; FtsZ; Sporulation; Streptomyces}},
language = {{eng}},
month = {{07}},
number = {{30}},
pages = {{6176--6183}},
publisher = {{National Academy of Sciences}},
series = {{Proceedings of the National Academy of Sciences of the United States of America}},
title = {{Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation}},
url = {{http://dx.doi.org/10.1073/pnas.1704612114}},
doi = {{10.1073/pnas.1704612114}},
volume = {{114}},
year = {{2017}},
}