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 Cell wall remodeling drives engulfment duringBacillus subtilissporulation

2016 ◽  
Author(s):  
Nikola Ojkic ◽  
Javier López-Garrido ◽  
Kit Pogliano ◽  
Robert G. Endres
Keyword(s):  
Cell Wall ◽  
Mother Cell ◽  
Asymmetric Cell Division ◽  
Leading Edge ◽  
Penicillin Binding Proteins ◽  
Cell Wall Remodeling ◽  
Biophysical Mechanism ◽  
A Cell ◽  
Lateral Cell ◽  
Synthesis And Degradation

AbstractWhen starved, the Gram-positive bacteriumBacillus subtilisforms 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 Distribution and preservation of the components of the engulfment. What is beyond representative genomes?

PLoS ONE ◽  
2021 ◽  
Vol 16 (3) ◽  
pp. e0246651
Author(s):  
Lizeth Soto-Avila ◽  
Ricardo Ciria Merce ◽  
Walter Santos ◽  
Nori Castañeda ◽  
Rosa-María Gutierrez-Ríos
Keyword(s):  
Bacillus Subtilis ◽  
Phylogenetic Reconstruction ◽  
Leading Edge ◽  
Extensive Study ◽  
Origin And Evolution ◽  
The Family ◽  
Family Level ◽  
Bioinformatic Approaches ◽  
Gain Loss ◽  
Synthesis And Degradation

Engulfment requires the coordinated, targeted synthesis and degradation of peptidoglycan at the leading edge of the engulfing membrane to allow the mother cell to completely engulf the forespore. Proteins such as the DMP and Q:AH complexes in Bacillus subtilis are essential for engulfment, as are a set of accessory proteins including GerM and SpoIIB, among others. Experimental and bioinformatic studies of these proteins in bacteria distinct from Bacillus subtilis indicate that fundamental differences exist regarding the organization and mechanisms used to successfully perform engulfment. As a consequence, the distribution and prevalence of the proteins involved in engulfment and other proteins that participate in different sporulation stages have been studied using bioinformatic approaches. These works are based on the prediction of orthologs in the genomes of representative Firmicutes and have been helpful in tracing hypotheses about the origin and evolution of sporulation genes, some of which have been postulated as sporulation signatures. To date, an extensive study of these signatures outside of the representative Firmicutes is not available. Here, we asked whether phyletic profiles of proteins involved in engulfment can be used as signatures able to describe the sporulation phenotype. We tested this hypothesis in a set of 954 Firmicutes, finding preserved phyletic profiles defining signatures at the genus level. Finally, a phylogenetic reconstruction based on non-redundant phyletic profiles at the family level shows the non-monophyletic origin of these proteins due to gain/loss events along the phylum Firmicutes.

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 Author response: Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

2016 ◽  
Author(s):  
Nikola Ojkic ◽  
Javier López-Garrido ◽  
Kit Pogliano ◽  
Robert G Endres
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Author Response ◽  
Cell Wall Remodeling

scholarly journals The lytE Gene of Bacillus subtilis 168 Encodes a Cell Wall Hydrolase

1998 ◽  
Vol 180 (8) ◽  
pp. 2272-2272
Author(s):  
Philippe Margot ◽  
Michael Whalen ◽  
Ahmad Gholamhoseinian ◽  
Patrick Piggot ◽  
Dimitri Karamata
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Bacillus Subtilis 168 ◽  
Cell Wall Hydrolase ◽  
A Cell

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 The influence of secretory-protein charge on late stages of secretion from the Gram-positive bacterium Bacillus subtilis

2000 ◽  
Vol 350 (1) ◽  
pp. 31-39 ◽  
Author(s):  
Keith STEPHENSON ◽  
Christina L. JENSEN ◽  
Steen T. JØRGENSEN ◽  
Jeremy H. LAKEY ◽  
Colin R. HARWOOD
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Culture Medium ◽  
Sequence Data ◽  
Chemical Properties ◽  
Secretory Protein ◽  
Secretory Proteins ◽  
Bacterium Bacillus Subtilis ◽  
Bacterium Bacillus ◽  
Late Stages

Following their secretion across the cytoplasmic membrane, processed secretory proteins of Bacillus subtilis must fold into their native conformation prior to translocation through the cell wall and release into the culture medium. The rate and efficiency of folding are critical in determining the yields of intact secretory proteins. The B. subtilis membrane is surrounded by a thick cell wall comprising a heteropolymeric matrix of peptidoglycan and anionic polymers. The latter confer a high density of negative charge on the wall, endowing it with ion-exchange properties, and secretory proteins destined for the culture medium must traverse the wall as the last stage in the export process. To determine the influence of charge on late stages in the secretion of proteins from this bacterium, we have used sequence data from two related α-amylases, to engineer the net charge of AmyL, an α-amylase from Bacillus licheniformis that is normally secreted efficiently from B. subtilis. While AmyL has a pI of 7.0, chimaeric enzymes with pI values of 5.0 and 10.0 were produced and characterized. Despite the engineered changes to their physico-chemical properties, the chimaeric enzymes retained many of the enzymic characteristics of AmyL. We show that the positively charged protein interacts with the cell wall in a manner that influences its secretion.

scholarly journals Muropeptide Rescue in Bacillus subtilis Involves Sequential Hydrolysis by β-N-Acetylglucosaminidase and N-Acetylmuramyl-l-Alanine Amidase

2010 ◽  
Vol 192 (12) ◽  
pp. 3132-3143 ◽  
Author(s):  
Silke Litzinger ◽  
Amanda Duckworth ◽  
Katja Nitzsche ◽  
Christian Risinger ◽  
Valentin Wittmann ◽  
...  
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
Stationary Phase ◽  
Particulate Material ◽  
Late Stationary Phase ◽  
Phosphotransferase System ◽  
E Coli ◽  
A Cell ◽  
Recycling Pathway ◽  
Hydrolysis Of

ABSTRACT We identified a pathway in Bacillus subtilis that is used for recovery of N-acetylglucosamine (GlcNAc)-N-acetylmuramic acid (MurNAc) peptides (muropeptides) derived from the peptidoglycan of the cell wall. This pathway is encoded by a cluster of six genes, the first three of which are orthologs of Escherichia coli genes involved in N-acetylmuramic acid dissimilation and encode a MurNAc-6-phosphate etherase (MurQ), a MurNAc-6-phosphate-specific transcriptional regulator (MurR), and a MurNAc-specific phosphotransferase system (MurP). Here we characterized two other genes of this cluster. The first gene was shown to encode a cell wall-associated β-N-acetylglucosaminidase (NagZ, formerly YbbD) that cleaves the terminal nonreducing N-acetylglucosamine of muropeptides and also accepts chromogenic or fluorogenic β-N-acetylglucosaminides. The second gene was shown to encode an amidase (AmiE, formerly YbbE) that hydrolyzes the N-acetylmuramyl-l-Ala bond of MurNAc peptides but not this bond of muropeptides. Hence, AmiE requires NagZ, and in conjunction these enzymes liberate MurNAc by sequential hydrolysis of muropeptides. NagZ expression was induced at late exponential phase, and it was 6-fold higher in stationary phase. NagZ is noncovalently associated with lysozyme-degradable particulate material and can be released from it with salt. A nagZ mutant accumulates muropeptides in the spent medium and displays a lytic phenotype in late stationary phase. The evidence for a muropeptide catabolic pathway presented here is the first evidence for cell wall recovery in a Gram-positive organism, and this pathway is distinct from the cell wall recycling pathway of E. coli and other Gram-negative bacteria.

Purification and crystallization of a cell wall recycling protein of Bacillus subtilis

2007 ◽  
Vol 2007 (Fall) ◽  
Author(s):  
Stefanie Fischer ◽  
Silke Litzinger ◽  
Christoph Mayer ◽  
Wolfram Welte
Keyword(s):  
Cell Wall ◽  
Bacillus Subtilis ◽  
A Cell ◽  
Cell Wall Recycling
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