scholarly journals Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor

Open Biology ◽  
2013 ◽  
Vol 3 (3) ◽  
pp. 130006 ◽  
Author(s):  
Bartosz Ditkowski ◽  
Neil Holmes ◽  
Joanna Rydzak ◽  
Magdalena Donczew ◽  
Martyna Bezulska ◽  
...  
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Tip Growth ◽  
Streptomyces Coelicolor ◽  
Proximal Region ◽  
Cytoskeletal Protein ◽  
Mutant Form ◽  
Bacterial Cell Division ◽  
Aerial Hyphae ◽  
Dynamic Interplay

Prior to bacterial cell division, the ATP-dependent polymerization of the cytoskeletal protein, ParA, positions the newly replicated origin-proximal region of the chromosome by interacting with ParB complexes assembled on parS sites located close to the origin. During the formation of unigenomic spores from multi-genomic aerial hyphae compartments of Streptomyces coelicolor , ParA is developmentally triggered to form filaments along the hyphae; this promotes the accurate and synchronized segregation of tens of chromosomes into prespore compartments. Here, we show that in addition to being a segregation protein, ParA also interacts with the polarity protein, Scy, which is a component of the tip-organizing centre that controls tip growth. Scy recruits ParA to the hyphal tips and regulates ParA polymerization. These results are supported by the phenotype of a strain with a mutant form of ParA that uncouples ParA polymerization from Scy. We suggest that the ParA–Scy interaction coordinates the transition from hyphal elongation to sporulation.

scholarly journals Streptomyces coelicolor Genes ftsL and divIC Play a Role in Cell Division but Are Dispensable for Colony Formation

2007 ◽  
Vol 189 (24) ◽  
pp. 8982-8992 ◽  
Author(s):  
Jennifer A. Bennett ◽  
Rachel M. Aimino ◽  
Joseph R. McCormick
Keyword(s):  
Cell Division ◽  
Double Mutant ◽  
Minimal Medium ◽  
Streptomyces Coelicolor ◽  
Bacterial Cell Division ◽  
Transmission Electron ◽  
Aerial Hyphae ◽  
Mutant Strains ◽  
High Sucrose ◽  
Insertion Mutations

ABSTRACT We have characterized homologues of the bacterial cell division genes ftsL and divIC in the gram-positive mycelial bacterium Streptomyces coelicolor A3(2). We show by deletion-insertion mutations that ftsL and divIC are dispensable for growth and viability in S. coelicolor. When mutant strains were grown on a conventional rich medium (R2YE, containing high sucrose), inactivation of either ftsL or divIC resulted in the formation of aerial hyphae with partially constricted division sites but no clear separation of prespore compartments. Surprisingly, this phenotype was largely suppressed when strains were grown on minimal medium or sucrose-free R2YE, where division sites in many aerial hyphae had finished constricting and chains of spores were evident. Thus, osmolarity appears to affect the severity of the division defect. Furthermore, double mutant strains deleted for both ftsL and divIC are viable and have medium-dependent phenotypes similar to that of the single mutant strains, suggesting that functions performed by FtsL and DivIC are not absolutely required for septation during growth and sporulation. Alternatively, another division protein may partially compensate for the loss of both FtsL and DivIC on minimal medium or sucrose-free R2YE. Finally, based on transmission electron microscopy observations, we propose that FtsL and DivIC are involved in coordinating symmetrical annular ingrowth of the invaginating septum.

scholarly journals Streptomyces: A Screening Tool for Bacterial Cell Division Inhibitors

2014 ◽  
Vol 20 (2) ◽  
pp. 275-284 ◽  
Author(s):  
Charul Jani ◽  
Elitza I. Tocheva ◽  
Scott McAuley ◽  
Arryn Craney ◽  
Grant J. Jensen ◽  
...  
Keyword(s):  
Cell Division ◽  
Stress Responses ◽  
Screening Tool ◽  
Streptomyces Coelicolor ◽  
Sos Response ◽  
Spore Formation ◽  
Bacterial Cell Division ◽  
Distinct Cell ◽  
Chemical Inhibitors ◽  
Complete Cell

Cell division is essential for spore formation but not for viability in the filamentous streptomycetes bacteria. Failure to complete cell division instead blocks spore formation, a phenotype that can be visualized by the absence of gray (in Streptomyces coelicolor) and green (in Streptomyces venezuelae) spore-associated pigmentation. Despite the lack of essentiality, the streptomycetes divisome is similar to that of other prokaryotes. Therefore, the chemical inhibitors of sporulation in model streptomycetes may interfere with the cell division in rod-shaped bacteria as well. To test this, we investigated 196 compounds that inhibit sporulation in S. coelicolor. We show that 19 of these compounds cause filamentous growth in Bacillus subtilis, consistent with impaired cell division. One of the compounds is a DNA-damaging agent and inhibits cell division by activating the SOS response. The remaining 18 act independently of known stress responses and may therefore act on the divisome or on divisome positioning and stability. Three of the compounds (Fil-1, Fil-2, and Fil-3) confer distinct cell division defects on B. subtilis. They also block B. subtilis sporulation, which is mechanistically unrelated to the sporulation pathway of streptomycetes but is also dependent on the divisome. We discuss ways in which these differing phenotypes can be used in screens for cell division inhibitors.

scholarly journals ZapA tetramerization is required for midcell localization and ZapB interaction in Escherichia coli

2019 ◽  
Author(s):  
Nils Y. Meiresonne ◽  
Tanneke den Blaauwen
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Resonance Energy Transfer ◽  
Resonance Energy ◽  
Bacterial Cell Division ◽  
Cellular Processes ◽  
Interaction Partners ◽  
Associated Proteins

AbstractBacterial cell division is guided by FtsZ treadmilling precisely at midcell. FtsZ itself is regulated by FtsZ associated proteins (Zaps) that couple it to different cellular processes. ZapA is known to enhance FtsZ bundling but also forms the synchronizing link with chromosome segregation through ZapB and matS bound MatP. ZapA exists as dimers and tetramers in the cell. Using the ZapAI83E mutant that only forms dimers, this paper investigates the effects of ZapA multimerization state on its interaction partners and cell division. By employing (fluorescence) microscopy and Förster Resonance Energy Transfer in vivo it is shown that; dimeric ZapA is unable to complement a zapA deletion strain and localizes diffusely through the cell but still interacts with FtsZ that is not part of the cell division machinery. Dimeric ZapA is unable to recruit ZapB, which localizes in its presence unipolarly in the cell. Interestingly, the localization profiles of the chromosome and unipolar ZapB anticorrelate. The work presented here confirms previously reported in vitro effects of ZapA multimerization in vivo and further places it in a broader context by revealing the strong implications for ZapB localization and ter linkage.

scholarly journals Branching of sporogenic aerial hyphae in sflA and sflB mutants of Streptomyces coelicolor correlates to ectopic localization of DivIVA and FtsZ in time and space

2020 ◽  
Author(s):  
Le Zhang ◽  
Joost Willemse ◽  
Paula Yagüe ◽  
Ellen de Waal ◽  
Dennis Claessen ◽  
...  
Keyword(s):  
Cell Division ◽  
Streptomyces Coelicolor ◽  
Constitutive Expression ◽  
Hyphal Growth ◽  
Lateral Wall ◽  
Specific Cell ◽  
Wild Type ◽  
Aerial Hyphae ◽  
In The Wild ◽  
Z Ring

ABSTRACTBacterial cytokinesis starts with the polymerization of the tubulin-like FtsZ, which forms the cell division scaffold. SepF aligns FtsZ polymers and also acts as a membrane anchor for the Z-ring. While in most bacteria cell division takes place at midcell, during sporulation of Streptomyces many septa are laid down almost simultaneously in multinucleoid aerial hyphae. The genomes of streptomycetes encode two additional SepF paralogs, SflA and SflB, which can interact with SepF. Here we show that the sporogenic aerial hyphae of sflA and sflB mutants of Streptomyces coelicolor frequently branch, a phenomenon never seen in the wild-type strain. The branching coincided with ectopic localization of DivIVA along the lateral wall of sporulating aerial hyphae. Constitutive expression of SflA and SflB largely inhibited hyphal growth, further correlating SflAB activity to that of DivIVA. SflAB localized in foci prior to and after the time of sporulation-specific cell division, while SepF co-localized with active septum synthesis. Foci of FtsZ and DivIVA frequently persisted between adjacent spores in spore chains of sflA and sflB mutants, at sites occupied by SflAB in wild-type cells. This may be caused by the persistance of SepF multimers in the absence of SflAB. Taken together, our data show that SflA and SflB play an important role in the control of growth and cell division during Streptomyces development.

scholarly journals Influence of CrgA on Assembly of the Cell Division Protein FtsZ during Development of Streptomyces coelicolor

2006 ◽  
Vol 188 (4) ◽  
pp. 1540-1550 ◽  
Author(s):  
Ricardo Del Sol ◽  
Jonathan G. L. Mullins ◽  
Nina Grantcharova ◽  
Klas Flärdh ◽  
Paul Dyson
Keyword(s):  
Cell Division ◽  
Streptomyces Coelicolor ◽  
Orthologous Gene ◽  
Integral Membrane Protein ◽  
Origin Of Replication ◽  
Small Proteins ◽  
Aerial Hyphae ◽  
Z Ring ◽  
Cell Division Protein ◽  
Conserved Gene

ABSTRACT The product of the crgA gene of Streptomyces coelicolor represents a novel family of small proteins. A single orthologous gene is located close to the origin of replication of all fully sequenced actinomycete genomes and borders a conserved gene cluster implicated in cell growth and division. In S. coelicolor, CrgA is important for coordinating growth and cell division in sporogenic hyphae. In this study, we demonstrate that CrgA is an integral membrane protein whose peak expression is coordinated with the onset of development of aerial hyphae. The protein localizes to discrete foci away from growing hyphal tips. Upon overexpression, CrgA localizes to apical syncytial cells of aerial hyphae and inhibits the formation of productive cytokinetic rings of the bacterial tubulin homolog FtsZ, leading to proteolytic turnover of this major cell division determinant. In the absence of known prokaryotic cell division inhibitors in actinomycetes, CrgA may have an important conserved function influencing Z-ring formation in these bacteria.

scholarly journals SMC Protein-Dependent Chromosome Condensation during Aerial Hyphal Development in Streptomyces

2008 ◽  
Vol 191 (1) ◽  
pp. 310-319 ◽  
Author(s):  
Agnieszka Kois ◽  
Magdalena Świątek ◽  
Dagmara Jakimowicz ◽  
Jolanta Zakrzewska-Czerwińska
Keyword(s):  
Chromosome Segregation ◽  
Joint Action ◽  
Streptomyces Coelicolor ◽  
Chromosome Condensation ◽  
Higher Order ◽  
Binary Fission ◽  
Vegetative Mycelium ◽  
Chromosome Dynamics ◽  
Aerial Hyphae ◽  
Smc Proteins

ABSTRACT Members of the SMC (structural maintenance of chromosomes) protein family play a central role in higher-order chromosome dynamics from bacteria to humans. So far, studies of bacterial SMC proteins have focused only on unicellular rod-shaped organisms that divide by binary fission. The conversion of multigenomic aerial hyphae of the mycelial organism Streptomyces coelicolor into chains of unigenomic spores requires the synchronous segregation of multiple chromosomes. Here we focus on the contribution of SMC proteins to sporulation-associated chromosome segregation in S. coelicolor. Deletion of the smc gene causes aberrant DNA condensation and missegregation of chromosomes (7.5% anucleate spores). In vegetative mycelium, immunostained SMC proteins were observed sporadically, while in aerial hyphae about to undergo sporulation they appeared as irregularly spaced foci which accompanied but did not colocalize with ParB complexes. Our data demonstrate that efficient chromosome segregation requires the joint action of SMC and ParB proteins. SMC proteins, similarly to ParAB and FtsZ, presumably belong to a larger group of proteins whose expression is highly induced in response to the requirement of aerial hyphal maturation.

scholarly journals Chromosome segregation drives division site selection inStreptococcus pneumoniae

2016 ◽  
Author(s):  
Renske van Raaphorst ◽  
Morten Kjos ◽  
Jan-Willem Veening
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Site Selection ◽  
Bacterial Cell Division ◽  
Division Plane ◽  
Canonical Systems ◽  
Daughter Cells ◽  
Division Site ◽  
Additional Protein ◽  
Site Control

AbstractAccurate spatial and temporal positioning of the tubulin-like protein FtsZ is key for proper bacterial cell division.Streptococcus pneumoniae(pneumococcus) is an oval-shaped, symmetrically dividing human pathogen lacking the canonical systems for division site control (nucleoid occlusion and the Min-system). Recently, the early division protein MapZ was identified and implicated in pneumococcal division site selection. We show that MapZ is important for proper division plane selection; thus the question remains what drives pneumococcal division site selection. By mapping the cell cycle in detail, we show that directly after replication both chromosomal origin regions localize to the future cell division sites, prior to FtsZ. Perturbing the longitudinal chromosomal organization by mutating the condensin SMC, by CRISPR/Cas9-mediated chromosome cutting or by poisoning DNA decatenation resulted in mistiming of MapZ and FtsZ positioning and subsequent cell elongation. Together, we demonstrate an intimate relationship between DNA replication, chromosome segregation and division site selection in the pneumococcus, providing a simple way to ensure equally sized daughter cells without the necessity for additional protein factors.

scholarly journals ¡vIVA la DivIVA!

2019 ◽  
Vol 201 (21) ◽  
Author(s):  
Lauren R. Hammond ◽  
Maria L. White ◽  
Prahathees J. Eswara
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Parental Cell ◽  
Model Organisms ◽  
Posttranslational Regulation ◽  
Bacterial Cell Division ◽  
Gram Positive ◽  
Content Type ◽  
Gram Positive Bacteria ◽  
Division Cell

ABSTRACT Reproduction in the bacterial kingdom predominantly occurs through binary fission—a process in which one parental cell is divided into two similarly sized daughter cells. How cell division, in conjunction with cell elongation and chromosome segregation, is orchestrated by a multitude of proteins has been an active area of research spanning the past few decades. Together, the monumental endeavors of multiple laboratories have identified several cell division and cell shape regulators as well as their underlying regulatory mechanisms in rod-shaped Escherichia coli and Bacillus subtilis, which serve as model organisms for Gram-negative and Gram-positive bacteria, respectively. Yet our understanding of bacterial cell division and morphology regulation is far from complete, especially in noncanonical and non-rod-shaped organisms. In this review, we focus on two proteins that are highly conserved in Gram-positive organisms, DivIVA and its homolog GpsB, and attempt to summarize the recent advances in this area of research and discuss their various roles in cell division, cell growth, and chromosome segregation in addition to their interactome and posttranslational regulation.

scholarly journals Assembly properties of FtsZ from cyanobacteriumSynechocystissp. PCC 6803

2019 ◽  
Author(s):  
Na Wang ◽  
Li Bian ◽  
Xueqin Ma ◽  
Yufeng Meng ◽  
Cyndi S. Chen ◽  
...  
Keyword(s):  
Cell Division ◽  
Bacterial Cell ◽  
Cytoskeletal Protein ◽  
Gtpase Activity ◽  
Bacterial Cell Division ◽  
Gtp Hydrolysis ◽  
Second Stage ◽  
Two Stages ◽  
Pcc 6803

ABSTRACTTubulin homologue FtsZ is the major cytoskeletal protein in the bacterial cell division machinery. Here, we studied the biochemical and assembly properties of SyFtsZ, FtsZ from cyanobacteriumSynechocystissp. PCC 6803. SyFtsZ had a slow GTPase activity of around 0.4 GTP per FtsZ per minute and assembled into thick, straight protofilament bundles and curved bundles designated toroids. The assembly of SyFtsZ in the presence of GTP occurred in two stages. The first stage was assembled into single straight protofilaments and opened circles; the second stage was association of the protofilaments into straight protofilament bundles and toroids. In addition to these assemblies in GTP, highly curved oligomers and minirings could be observed after GTP hydrolysis or in the presence of GDP. Those three types of protofilaments of SyFtsZ provide support for the hypothesis for a constriction force based on curved protofilaments.

scholarly journals Deacetylation enhances ParB–DNA interactions affecting chromosome segregation in Streptomyces coelicolor

2020 ◽  
Vol 48 (9) ◽  
pp. 4902-4914
Author(s):  
Peng Li ◽  
Hong Zhang ◽  
Guo-Ping Zhao ◽  
Wei Zhao
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Direct Evidence ◽  
Streptomyces Coelicolor ◽  
Cell Metabolism ◽  
Lysine Acetylation ◽  
Biological Processes ◽  
Dna Interactions ◽  
Dna Binding Affinity ◽  
Metabolism Gene

Abstract Reversible lysine acetylation plays regulatory roles in diverse biological processes, including cell metabolism, gene transcription, cell apoptosis and ageing. Here, we show that lysine acetylation is involved in the regulation of chromosome segregation, a pivotal step during cell division in Streptomyces coelicolor. Specifically, deacetylation increases the DNA-binding affinity of the chromosome segregation protein ParB to the centromere-like sequence parS. Both biochemical and genetic experiments suggest that the deacetylation process is mainly modulated by a sirtuin-like deacetylase ScCobB1. The Lys-183 residue in the helix-turn-helix region of ParB is the major deacetylation site responsible for the regulation of ParB-parS binding. In-frame deletion of SccobB1 represses formation of ParB segregation complexes and leads to generation of abnormal spores. Taken together, these observations provide direct evidence that deacetylation participates in the regulation of chromosome segregation by targeting ParB in S. coelicolor.

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