Two dynamin-like proteins stabilize FtsZ rings during Streptomyces sporulation

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 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.he active organization and remodeling of cellular membranes is a fundamental process for all organisms. Many of these remodeling events involve the reshaping, fission, or fusion of lipid bilayers to generate new organelles, release transport vesicles, or stabilize specific membrane structures. In eukaryotes, key cellular processes, such as the fission and fusion of mitochondria, the division of chloroplasts, endocytosis, and viral resistance, are mediated by members of the dynamin superfamily (1). Dynamins and dynamin-like proteins are mechanochemical GTPases that polymerize into helical scaffolds at the surface of membranes. GTP hydrolysis is coupled to a radical conformational change in the protein structure that forces the underlying lipid layer into an energetically unstable conformation that promotes membrane rearrangements, probably via a hemifusion intermediate (2, 3).Dynamin-like proteins are found in many bacterial species, yet the precise roles of these proteins are still largely unknown. They share a conserved domain architecture with the canonical human Dynamin 1, including the N-terminal GTPase domain, a neck domain involved in dynamin dimerization, and a trunk domain involved in stimulation of GTPase activity (4, 5). In contrast, bacterial dynamins lack the pleckstrin homology motif and proline-rich sequences found in classical dynamins and contain instead o...

Dynamin-like proteins are essential for vesicle biogenesis inMycobacterium tuberculosis

“…Dynamin, the founding member of this family, mediates membrane fission leading to the budding of vesicles during endocytosis (29). Bacterial DLPs are poorly understood, but they appear to function in a variety of processes: Escherichia coli CrfC functions in chromosome partitioning during DNA replication (30), DynA and DynB in Streptomyces are involved in cell division during sporulation (31), DynA in Bacillus subtillis can tether membranes and may mediate membrane repair (32), and LeoA, B and C in enterogenic E. coli localize to the periplasm and contribute to virulence through membrane vesicle associated toxin secretion (33).…”

MADS‐box transcription factor Mcm1 controls cell cycle, fungal development, cell integrity and virulence in the filamentous insect pathogenic fungus Beauveria bassiana

“…Dynamics are a family of large, multidomain GTPases involved in key cellular processes in eukaryotes, including vesicle trafficking and organelle division (Ferguson and De Camilli, 2012). Recently, two Streptomyces dynamins are found to specifically localize to sporulation septa in an FtsZdependent manner and are crucial for septum synthesis during sporulation (Schlimpert et al, 2017). Since transcription patterns of two dynamin family protein genes (BBA_07980 and BBA_10077) were distinctly altered in the mutants, we reasonably speculate that the two genes might be involved in septum formation of B. bassiana.…”

“…Additional DEGs were involved in energy (9), protein fate (11), cell rescue, defence and virulence (25), cellular transport, transport facilities and transport routes (14), cellular communication (12) and transcription (2) (Supporting Information Table S2). Of those DEGs, four genes were probably involved in septum formation and/or sporulation, which encoded SCF E3 ubiquitin ligase complex F-box protein grrA (BBA_09932) (Corbett et al, 2006), casein kinase 1 epsilon (BBA_06604) (Robinson et al, 1999), dynamin GTPase (BBA_07980) and dynamin family protein (BBA_10077) (Schlimpert et al, 2017).…”

Specialized and shared functions of diguanylate cyclases and phosphodiesterases inStreptomycesdevelopment

“…(B) Fluorescence (left) and phase contrast microscopy images (right) showing that FtsZ-YPet is upregulated in Δ cdgB and Δ cdgC after 12 h of growth in liquid MYM. FtsZ-YPet was expressed from the Φ BT1 integration site under control of the native ftsZ promoter from the pSS5 vector (40). (C) Immunoblot analysis using anti-GFP antibody for FtsZ-YPet detection.…”