Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation

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Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation. / Schlimpert, Susan; Wasserstrom, Sebastian; Chandra, Govind; Bibb, Maureen J.; Findlay, Kim C.; Flärdh, Klas; Buttner, Mark J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 30, 25.07.2017, p. E6176-E6183.

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Schlimpert, Susan ; Wasserstrom, Sebastian ; Chandra, Govind ; Bibb, Maureen J. ; Findlay, Kim C. ; Flärdh, Klas ; Buttner, Mark J. / Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 30. pp. E6176-E6183.

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TY - JOUR

T1 - Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation

AU - Schlimpert, Susan

AU - Wasserstrom, Sebastian

AU - Chandra, Govind

AU - Bibb, Maureen J.

AU - Findlay, Kim C.

AU - Flärdh, Klas

AU - Buttner, Mark J.

PY - 2017/7/25

Y1 - 2017/7/25

N2 - 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.

AB - 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.

KW - Bacterial dynamins

KW - Cell division

KW - FtsZ

KW - Sporulation

KW - Streptomyces

U2 - 10.1073/pnas.1704612114

DO - 10.1073/pnas.1704612114

M3 - Article

VL - 114

SP - E6176-E6183

JO - Proceedings of the National Academy of Sciences

T2 - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

SN - 1091-6490

IS - 30

ER -