Advanced

Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation

Schlimpert, Susan; Wasserstrom, Sebastian LU ; Chandra, Govind; Bibb, Maureen J.; Findlay, Kim C.; Flärdh, Klas LU and Buttner, Mark J. (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.

(Less)
Please use this url to cite or link to this publication:
author
organization
publishing date
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 Acad Sciences
external identifiers
  • scopus:85025670503
  • wos:000406189900020
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
2017-09-18 11:40:43
@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},
  keyword      = {Bacterial dynamins,Cell division,FtsZ,Sporulation,Streptomyces},
  language     = {eng},
  month        = {07},
  number       = {30},
  pages        = {6176--6183},
  publisher    = {National Acad 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},
  volume       = {114},
  year         = {2017},
}