scholarly journals Postdivisional Synthesis of the Sporosarcina ureae DNA Translocase SpoIIIE either in the Mother Cell or in the Prespore Enables Bacillus subtilis To Translocate DNA from the Mother Cell to the Prespore

2003 ◽  
Vol 185 (3) ◽  
pp. 879-886 ◽  
Author(s):  
Vasant K. Chary ◽  
Patrick J. Piggot
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Mother Cell ◽  
Asymmetric Cell Division ◽  
Dna Translocation ◽  
Sporosarcina Ureae ◽  
Correct Orientation ◽  
Chromosome Partitioning ◽  
Specific Synthesis ◽  
Dna Translocase

ABSTRACT The differentiation of vegetative cells of Bacillus subtilis into spores involves asymmetric cell division, which precedes complete chromosome partitioning. The DNA translocase SpoIIIE is required to translocate the origin distal 70% of the chromosome from the larger mother cell into the smaller prespore, the two cells that result from the division. We have tested the effect of altering the time and location of SpoIIIE synthesis on spore formation. We have expressed the spoIIIE homologue from Sporosarcina ureae in B. subtilis under the control of different promoters. Expression from either a weak mother cell-specific (σE) promoter or a weak prespore-specific (σF) promoter partly complemented the sporulation defect of a spoIIIE36 mutant; however, expression from a strong prespore-specific (σF) promoter did not. DNA translocation from the mother cell to the prespore was assayed using spoIIQ-lacZ inserted at thrC; transcription of spoIIQ occurs only in the prespore. Translocation of thrC::spoIIQ-lacZ into the prespore occurred efficiently when spoIIIE Su was expressed from the weak σE- or σF-controlled promoters but not when it was expressed from the strong σF-controlled promoter. It is speculated that the mechanism directing SpoIIIE insertion into the septum in the correct orientation may accommodate slow postseptational, prespore-specific SpoIIIE synthesis but may be swamped by strong prespore-specific synthesis.

scholarly journals Partitioning of Chromosomal DNA during Establishment of Cellular Asymmetry in Bacillus subtilis

2002 ◽  
Vol 184 (6) ◽  
pp. 1743-1749 ◽  
Author(s):  
Joe Pogliano ◽  
Marc D. Sharp ◽  
Kit Pogliano
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Asymmetric Cell Division ◽  
Chromosome Structure ◽  
Chromosomal Dna ◽  
Chromosome Partitioning ◽  
Cellular Asymmetry ◽  
The Future ◽  
Asymmetric Partitioning ◽  
Polar Division

ABSTRACT The switch from symmetric to asymmetric cell division is a key feature of development in many organisms, including Bacillus subtilis sporulation. Here we demonstrate that, prior to the onset of asymmetric cell division, the B. subtilis chromosome is partitioned into two unequally sized domains, with the origin-proximal one-third of the future forespore chromosome condensed near one pole of the cell. Asymmetric chromosome partitioning is independent of polar division, as it occurs in cells depleted of FtsZ but depends on two transcription factors that govern the initiation of sporulation, σH and Spo0A-P. It is also independent of chromosome partitioning proteins Spo0J and Soj, suggesting the existence of a novel mechanism controlling chromosome structure. Thus, our results demonstrate that, during sporulation, two separable events prepare B. subtilis for asymmetric cell division: the relocation of cell division sites to the cell poles and the asymmetric partitioning of the future forespore chromosome.

scholarly journals Membrane fission during bacterial spore development requires DNA-driven cellular inflation

2021 ◽  
Author(s):  
Ane Landajuela ◽  
Martha Braun ◽  
Alejandro Martinez-Calvo ◽  
Christopher D. A. Rodrigues ◽  
Thierry Doan ◽  
...  
Keyword(s):  
Cell Division ◽  
Mother Cell ◽  
Complete Genome ◽  
Molecular Basis ◽  
Membrane Tension ◽  
Dna Translocation ◽  
Cell Cytoplasm ◽  
Membrane Fission ◽  
Catalyzed Membrane ◽  
Dna Translocase

Bacteria require membrane fission for cell division and endospore formation. FisB catalyzes membrane fission during sporulation, but the molecular basis is unclear as it cannot remodel membranes by itself. Sporulation initiates with an asymmetric division that generates a large mother cell and a smaller forespore that contains only 1/4 of its complete genome. As the mother cell membranes engulf the forespore, a DNA translocase pumps the rest of the chromosome into the small forespore compartment, inflating it due to increased turgor. When the engulfing membranes undergo fission, the forespore is released into the mother cell cytoplasm. Here we show that forespore inflation and FisB accumulation are both required for efficient membrane fission. We suggest that high membrane tension in the engulfment membrane caused by forespore inflation drives FisB-catalyzed membrane fission. Collectively our data indicate that DNA-translocation has a previously unappreciated second function in energizing FisB-mediated membrane fission under energy-limited conditions.

scholarly journals Contrasting Effects of σE on Compartmentalization of σF Activity during Sporulation of Bacillus subtilis

2004 ◽  
Vol 186 (7) ◽  
pp. 1983-1990 ◽  
Author(s):  
David W. Hilbert ◽  
Vasant K. Chary ◽  
Patrick J. Piggot
Keyword(s):  
Gene Expression ◽  
Transcription Factor ◽  
Bacillus Subtilis ◽  
Mother Cell ◽  
Cell Fates ◽  
Gene Encoding ◽  
Primitive Form ◽  
Small Proteins ◽  
Dna Translocase

ABSTRACT Spore formation by Bacillus subtilis is a primitive form of development. In response to nutrient starvation and high cell density, B. subtilis divides asymmetrically, resulting in two cells with different sizes and cell fates. Immediately after division, the transcription factor σF becomes active in the smaller prespore, which is followed by the activation of σE in the larger mother cell. In this report, we examine the role of the mother cell-specific transcription factor σE in maintaining the compartmentalization of gene expression during development. We have studied a strain with a deletion of the spoIIIE gene, encoding a DNA translocase, that exhibits uncompartmentalized σF activity. We have determined that the deletion of spoIIIE alone does not substantially impact compartmentalization, but in the spoIIIE mutant, the expression of putative peptidoglycan hydrolases under the control of σE in the mother cell destroys the integrity of the septum. As a consequence, small proteins can cross the septum, thereby abolishing compartmentalization. In addition, we have found that in a mutant with partially impaired control of σF, the activation of σE in the mother cell is important to prevent the activation of σF in this compartment. Therefore, the activity of σE can either maintain or abolish the compartmentalization of σF, depending upon the genetic makeup of the strain. We conclude that σE activity must be carefully regulated in order to maintain compartmentalization of gene expression during development.

scholarly journals Asymmetric localization of the cell division machinery during Bacillus subtilis sporulation

2020 ◽  
Author(s):  
Kanika Khanna ◽  
Javier López-Garrido ◽  
Joseph Sugie ◽  
Kit Pogliano ◽  
Elizabeth Villa
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Vegetative Growth ◽  
Bacterial Cell ◽  
Mother Cell ◽  
Electron Tomography ◽  
Leading Edge ◽  
Specific Protein ◽  
Bacterial Cell Division ◽  
Division Plane

The mechanistic details of bacterial cell division are poorly understood. The Gram-positive bacterium Bacillus subtilis can divide via two modes. During vegetative growth, the division septum is formed at the mid cell to produce two equal daughter cells. However, during sporulation, the division septum is formed closer to one pole to yield a smaller forespore and a larger mother cell. We use cryo-electron tomography to visualize the architectural differences in the organization of FtsAZ filaments, the major orchestrators of bacterial cell division during these conditions. We demonstrate that during vegetative growth, FtsAZ filaments are present uniformly around the leading edge of the invaginating septum but during sporulation, they are only present on the mother cell side. Our data show that the sporulation septum is thinner than the vegetative septum during constriction, and that this correlates with half as many FtsZ filaments tracking the division plane during sporulation as compared to vegetative growth. We further find that a sporulation-specific protein, SpoIIE, regulates divisome localization and septal thickness during sporulation. Our data provide first evidence of asymmetric localization of the cell division machinery, and not just septum formation, to produce different cell types with diverse fates in bacteria.

scholarly journals Separation of Chromosome Termini during Sporulation of Bacillus subtilis Depends on SpoIIIE

2007 ◽  
Vol 189 (9) ◽  
pp. 3564-3572 ◽  
Author(s):  
Marina Bogush ◽  
Panagiotis Xenopoulos ◽  
Patrick J. Piggot
Keyword(s):  
Bacillus Subtilis ◽  
Vegetative Growth ◽  
Mother Cell ◽  
Spore Formation ◽  
The Other ◽  
Septum Formation ◽  
Chromosome Separation ◽  
Dna Translocase

ABSTRACT Bacillus subtilis undergoes a highly distinctive division during spore formation. It yields two unequal cells, the mother cell and the prespore, and septum formation is completed before the origin-distal 70% of the chromosome has entered the smaller prespore. The mother cell subsequently engulfs the prespore. Two different probes were used to study the behavior of the terminus (ter) region of the chromosome during spore formation. Only one ter region was observed at the time of sporulation division. A second ter region, indicative of chromosome separation, was not distinguishable until engulfment was nearing completion, when one was in the mother cell and the other in the prespore. Separation of the two ter regions depended on the DNA translocase SpoIIIE. It is concluded that SpoIIIE is required during spore formation for chromosome separation as well as for translocation; SpoIIIE is not required for separation during vegetative growth.

scholarly journals The Role of Cytoplasmic MEX-5/6 Polarity in Asymmetric Cell Division

2021 ◽  
Vol 83 (4) ◽  
Author(s):  
Sungrim Seirin-Lee
Keyword(s):  
Mathematical Model ◽  
Cell Division ◽  
Caenorhabditis Elegans ◽  
Cell Membrane ◽  
Mother Cell ◽  
Asymmetric Cell Division ◽  
Transmembrane Protein ◽  
Cytoplasmic Protein ◽  
Cell Geometry

AbstractIn the process of asymmetric cell division, the mother cell induces polarity in both the membrane and the cytosol by distributing substrates and components asymmetrically. Such polarity formation results from the harmonization of the upstream and downstream polarities between the cell membrane and the cytosol. MEX-5/6 is a well-investigated downstream cytoplasmic protein, which is deeply involved in the membrane polarity of the upstream transmembrane protein PAR in the Caenorhabditis elegans embryo. In contrast to the extensive exploration of membrane PAR polarity, cytoplasmic polarity is poorly understood, and the precise contribution of cytoplasmic polarity to the membrane PAR polarity remains largely unknown. In this study, we explored the interplay between the cytoplasmic MEX-5/6 polarity and the membrane PAR polarity by developing a mathematical model that integrates the dynamics of PAR and MEX-5/6 and reflects the cell geometry. Our investigations show that the downstream cytoplasmic protein MEX-5/6 plays an indispensable role in causing a robust upstream PAR polarity, and the integrated understanding of their interplay, including the effect of the cell geometry, is essential for the study of polarity formation in asymmetric cell division.

scholarly journals Asymmetric localization of the cell division machinery during Bacillus subtilis sporulation

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Kanika Khanna ◽  
Javier Lopez Garrido ◽  
Joseph Sugie ◽  
Kit Pogliano ◽  
Elizabeth Villa
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Mother Cell ◽  
Electron Tomography ◽  
Leading Edge ◽  
Specific Protein ◽  
Bacterial Cell Division ◽  
Daughter Cells ◽  
Septal Thickness ◽  
Cryo Electron Tomography

The Gram-positive bacterium Bacillus subtilis can divide via two modes. During vegetative growth, the division septum is formed at the midcell to produce two equal daughter cells. However, during sporulation, the division septum is formed closer to one pole to yield a smaller forespore and a larger mother cell. Using cryo-electron tomography, genetics and fluorescence microscopy, we found that the organization of the division machinery is different in the two septa. While FtsAZ filaments, the major orchestrators of bacterial cell division, are present uniformly around the leading edge of the invaginating vegetative septa, they are only present on the mother cell side of the invaginating sporulation septa. We provide evidence suggesting that the different distribution and number of FtsAZ filaments impact septal thickness, causing vegetative septa to be thicker than sporulation septa already during constriction. Finally, we show that a sporulation-specific protein, SpoIIE, regulates asymmetric divisome localization and septal thickness during sporulation.

scholarly journals Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Nikola Ojkic ◽  
Javier López-Garrido ◽  
Kit Pogliano ◽  
Robert G Endres
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Mother Cell ◽  
Asymmetric Cell Division ◽  
Leading Edge ◽  
Cell Wall Remodeling ◽  
Biophysical Mechanism ◽  
A Cell ◽  
Bacterium Bacillus ◽  
Synthesis And Degradation

When starved, the Gram-positive bacterium Bacillus subtilis forms durable spores for survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosis-like process. However, the force generation mechanism for forward membrane movement remains unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by penicillin binding proteins in the forespore and a cell wall degradation protein complex in the mother cell. We propose a simple model for engulfment in which the junction between the septum and the lateral cell wall moves around the forespore by a mechanism resembling the ‘template model’. Hence, we establish a biophysical mechanism for the creation of a force for engulfment based on the coordination between cell wall synthesis and degradation.

scholarly journals Linking the Peptidoglycan Synthesis Protein Complex with Asymmetric Cell Division during Bacillus subtilis Sporulation

2020 ◽  
Vol 21 (12) ◽  
pp. 4513 ◽  
Author(s):  
Katarína Muchová ◽  
Zuzana Chromiková ◽  
Imrich Barák
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Protein Complex ◽  
Asymmetric Cell Division ◽  
Morphological Changes ◽  
Direct Interaction ◽  
Specific Protein ◽  
Peptidoglycan Biosynthesis ◽  
Peptidoglycan Synthesis ◽  
Septum Formation

Peptidoglycan is generally considered one of the main determinants of cell shape in bacteria. In rod-shaped bacteria, cell elongation requires peptidoglycan synthesis to lengthen the cell wall. In addition, peptidoglycan is synthesized at the division septum during cell division. Sporulation of Bacillus subtilis begins with an asymmetric cell division. Formation of the sporulation septum requires almost the same set of proteins as the vegetative septum; however, these two septa are significantly different. In addition to their differences in localization, the sporulation septum is thinner and it contains SpoIIE, a crucial sporulation specific protein. Here we show that peptidoglycan biosynthesis is linked to the cell division machinery during sporulation septum formation. We detected a direct interaction between SpoIIE and GpsB and found that both proteins co-localize during the early stages of asymmetric septum formation. We propose that SpoIIE is part of a multi-protein complex which includes GpsB, other division proteins and peptidoglycan synthesis proteins, and could provide a link between the peptidoglycan synthesis machinery and the complex morphological changes required for forespore formation during B. subtilis sporulation.

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