scholarly journals FtsEX-mediated regulation of inner membrane fusion and cell separation reveals morphogenetic plasticity inCaulobacter crescentus

2017 ◽  
Author(s):  
Elizabeth L. Meier ◽  
Qing Yao ◽  
Allison K. Daitch ◽  
Grant J. Jensen ◽  
Erin D. Goley
Keyword(s):  
Cell Wall ◽  
Membrane Fusion ◽  
Bacterial Cell ◽  
Cell Separation ◽  
Cell Shape ◽  
Caulobacter Crescentus ◽  
Inner Membrane ◽  
Bacterial Cell Shape ◽  
Late Stages ◽  
Shape Changes

AbstractDuring its life cycle,Caulobacter crescentusundergoes a series of coordinated shape changes, including generation of a polar stalk and reshaping of the cell envelope to produce new daughter cells through the process of cytokinesis. The mechanisms by which these morphogenetic processes are coordinated in time and space remain largely unknown. Here we demonstrate that the conserved division complex FtsEX controls both the early and late stages of cytokinesis inC. crescentus, namely initiation of constriction and final cell separation. ΔftsEcells display a striking phenotype: cells are chained, with skinny connections between cell bodies resulting from defects in inner membrane fusion and cell separation. Surprisingly, the thin connections in ΔftsEcells share morphological and molecular features withC. crescentusstalks. Our data uncover unanticipated morphogenetic plasticity inC. crescentus, with loss of FtsE causing a stalk-like program to take over at failed division sites and yield novel cell morphology.Author SummaryBacterial cell shape is genetically hardwired and is critical for fitness and, in certain cases, pathogenesis. In most bacteria, a semi-rigid structure called the cell wall surrounds the inner membrane, offering protection against cell lysis while simultaneously maintaining cell shape. A highly dynamic macromolecular structure, the cell wall undergoes extensive remodeling as bacterial cells grow and divide. We demonstrate that a broadly conserved cell division complex, FtsEX, relays signals from the cytoplasm to the cell wall to regulate key developmental shape changes in the α-proteobacteriumCaulobacter crescentus. Consistent with studies in diverse bacteria, we observe strong synthetic interactions betweenftsEand cell wall hydrolytic factors, suggesting that regulation of cell wall remodeling is a conserved function of FtsEX. Loss of FtsE causes morphological defects associated with both the early and late stages of division. Intriguingly, without FtsE, cells frequently fail to separate and instead elaborate a thin, tubular structure between cell bodies, a growth mode observed in other α-proteobacteria. Overall, our results highlight the plasticity of bacterial cell shape and demonstrate how altering the activity of one morphogenetic program can produce diverse morphologies resembling those of other bacteria in nature.

scholarly journals Bacterial Cell Wall Synthesis: New Insights from Localization Studies

2005 ◽  
Vol 69 (4) ◽  
pp. 585-607 ◽  
Author(s):  
Dirk-Jan Scheffers ◽  
Mariana G. Pinho
Keyword(s):  
Cell Wall ◽  
Bacterial Cell ◽  
Cell Shape ◽  
Fluorescent Protein ◽  
Model Organisms ◽  
Live Cells ◽  
Cell Wall Synthesis ◽  
A Cell ◽  
Green Fluorescent ◽  
Bacterial Cell Shape

SUMMARY In order to maintain shape and withstand intracellular pressure, most bacteria are surrounded by a cell wall that consists mainly of the cross-linked polymer peptidoglycan (PG). The importance of PG for the maintenance of bacterial cell shape is underscored by the fact that, for various bacteria, several mutations affecting PG synthesis are associated with cell shape defects. In recent years, the application of fluorescence microscopy to the field of PG synthesis has led to an enormous increase in data on the relationship between cell wall synthesis and bacterial cell shape. First, a novel staining method enabled the visualization of PG precursor incorporation in live cells. Second, penicillin-binding proteins (PBPs), which mediate the final stages of PG synthesis, have been localized in various model organisms by means of immunofluorescence microscopy or green fluorescent protein fusions. In this review, we integrate the knowledge on the last stages of PG synthesis obtained in previous studies with the new data available on localization of PG synthesis and PBPs, in both rod-shaped and coccoid cells. We discuss a model in which, at least for a subset of PBPs, the presence of substrate is a major factor in determining PBP localization.

scholarly journals The evolution of spherical cell shape; progress and perspective

2019 ◽  
Vol 47 (6) ◽  
pp. 1621-1634 ◽  
Author(s):  
Paul Richard Jesena Yulo ◽  
Heather Lyn Hendrickson
Keyword(s):  
Cell Wall ◽  
Bacterial Cell ◽  
Cell Shape ◽  
Shape Change ◽  
Spherical Cell ◽  
Shape Evolution ◽  
Penicillin Binding Proteins ◽  
Cell Shape Change ◽  
Peptidoglycan Cell Wall ◽  
Bacterial Cell Shape

Bacterial cell shape is a key trait governing the extracellular and intracellular factors of bacterial life. Rod-like cell shape appears to be original which implies that the cell wall, division, and rod-like shape came together in ancient bacteria and that the myriad of shapes observed in extant bacteria have evolved from this ancestral shape. In order to understand its evolution, we must first understand how this trait is actively maintained through the construction and maintenance of the peptidoglycan cell wall. The proteins that are primarily responsible for cell shape are therefore the elements of the bacterial cytoskeleton, principally FtsZ, MreB, and the penicillin-binding proteins. MreB is particularly relevant in the transition between rod-like and spherical cell shape as it is often (but not always) lost early in the process. Here we will highlight what is known of this particular transition in cell shape and how it affects fitness before giving a brief perspective on what will be required in order to progress the field of cell shape evolution from a purely mechanistic discipline to one that has the perspective to both propose and to test reasonable hypotheses regarding the ecological drivers of cell shape change.

scholarly journals Bacterial Cell Wall Quality Control during Environmental Stress

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Elizabeth A. Mueller ◽  
Petra Anne Levin
Keyword(s):  
Quality Control ◽  
Cell Wall ◽  
Cell Surface ◽  
Environmental Stress ◽  
Environmental Conditions ◽  
Bacterial Cell ◽  
Cell Shape ◽  
Bacterial Cell Wall ◽  
Peptidoglycan Synthesis ◽  
Peptidoglycan Cell Wall

ABSTRACT Single-celled organisms must adapt their physiology to persist and propagate across a wide range of environmental conditions. The growth and division of bacterial cells depend on continuous synthesis of an essential extracellular barrier: the peptidoglycan cell wall, a polysaccharide matrix that counteracts turgor pressure and confers cell shape. Unlike many other essential processes and structures within the bacterial cell, the peptidoglycan cell wall and its synthesis machinery reside at the cell surface and are thus uniquely vulnerable to the physicochemical environment and exogenous threats. In addition to the diversity of stressors endangering cell wall integrity, defects in peptidoglycan metabolism require rapid repair in order to prevent osmotic lysis, which can occur within minutes. Here, we review recent work that illuminates mechanisms that ensure robust peptidoglycan metabolism in response to persistent and acute environmental stress. Advances in our understanding of bacterial cell wall quality control promise to inform the development and use of antimicrobial agents that target the synthesis and remodeling of this essential macromolecule. IMPORTANCE Nearly all bacteria are encased in a peptidoglycan cell wall, an essential polysaccharide structure that protects the cell from osmotic rupture and reinforces cell shape. The integrity of this protective barrier must be maintained across the diversity of environmental conditions wherein bacteria replicate. However, at the cell surface, the cell wall and its synthesis machinery face unique challenges that threaten their integrity. Directly exposed to the extracellular environment, the peptidoglycan synthesis machinery encounters dynamic and extreme physicochemical conditions, which may impair enzymatic activity and critical protein-protein interactions. Biotic and abiotic stressors—including host defenses, cell wall active antibiotics, and predatory bacteria and phage—also jeopardize peptidoglycan integrity by introducing lesions, which must be rapidly repaired to prevent cell lysis. Here, we review recently discovered mechanisms that promote robust peptidoglycan synthesis during environmental and acute stress and highlight the opportunities and challenges for the development of cell wall active therapeutics.

Bacterial Cell Shape–Dependent Inflammatory Response in Mammary Epithelial Cells

2006 ◽  
Vol 52 (6) ◽  
pp. 424-429 ◽  
Author(s):  
Medhat M. Khattar ◽  
Samer Bazzi ◽  
Joanna Kogan ◽  
Rabih S. Talhouk
Keyword(s):  
Epithelial Cells ◽  
Inflammatory Response ◽  
Bacterial Cell ◽  
Cell Shape ◽  
Mammary Epithelial Cells ◽  
Mammary Epithelial ◽  
Bacterial Cell Shape

Biophysical Measurements of Bacterial Cell Shape

2016 ◽  
pp. 227-245 ◽  
Author(s):  
Jeffrey P. Nguyen ◽  
Benjamin P. Bratton ◽  
Joshua W. Shaevitz
Keyword(s):  
Bacterial Cell ◽  
Cell Shape ◽  
Bacterial Cell Shape

scholarly journals Genetic mechanism regulating bacterial cell shape and metabolism

2009 ◽  
Vol 2 (3) ◽  
pp. 219-220 ◽  
Author(s):  
Daisuke Shiomi ◽  
Hideo Mori ◽  
Hironori Niki
Keyword(s):  
Bacterial Cell ◽  
Cell Shape ◽  
Genetic Mechanism ◽  
Bacterial Cell Shape

scholarly journals Sugar-Phosphate Metabolism Regulates Stationary-Phase Entry and Stalk Elongation in Caulobacter crescentus

2019 ◽  
Vol 202 (4) ◽  
Author(s):  
Kevin D. de Young ◽  
Gabriele Stankeviciute ◽  
Eric A. Klein
Keyword(s):  
Stationary Phase ◽  
Cell Shape ◽  
Caulobacter Crescentus ◽  
Phosphate Starvation ◽  
Phosphomannose Isomerase ◽  
Sugar Phosphate ◽  
Content Type ◽  
Environmental Perturbations ◽  
Bacterial Cell Shape ◽  
Phase Entry

ABSTRACT Bacteria have a variety of mechanisms for adapting to environmental perturbations. Changes in oxygen availability result in a switch between aerobic and anaerobic respiration, whereas iron limitation may lead to siderophore secretion. In addition to metabolic adaptations, many organisms respond by altering their cell shape. Caulobacter crescentus, when grown under phosphate-limiting conditions, dramatically elongates its polar stalk appendage. The stalk is hypothesized to facilitate phosphate uptake; however, the mechanistic details of stalk synthesis are not well characterized. We used a chemical mutagenesis approach to isolate and characterize stalk-deficient mutants, one of which had two mutations in the phosphomannose isomerase gene (manA) that were necessary and sufficient to inhibit stalk elongation. Transcription of the pho regulon was unaffected in the manA mutant; therefore, ManA plays a unique regulatory role in stalk synthesis. The mutant ManA had reduced enzymatic activity, resulting in a 5-fold increase in the intracellular fructose 6-phosphate/mannose 6-phosphate ratio. This metabolic imbalance impaired the synthesis of cellular envelope components derived from mannose 6-phosphate, namely, lipopolysaccharide O-antigen and exopolysaccharide. Furthermore, the manA mutations prevented C. crescentus cells from efficiently entering stationary phase. Deletion of the stationary-phase response regulator gene spdR inhibited stalk elongation in wild-type cells, while overproduction of the alarmone ppGpp, which triggers growth arrest and stationary-phase entry, increased stalk length in the manA mutant strain. These results demonstrate that sugar-phosphate metabolism regulates stalk elongation independently of phosphate starvation. IMPORTANCE Metabolic control of bacterial cell shape is an important mechanism for adapting to environmental perturbations. Caulobacter crescentus dramatically elongates its polar stalk appendage in response to phosphate starvation. To investigate the mechanism of this morphological adaptation, we isolated stalk-deficient mutants, one of which had mutations in the phosphomannose isomerase gene (manA) that blocked stalk elongation, despite normal activation of the phosphate starvation response. The mutant ManA resulted in an imbalance in sugar-phosphate concentrations, which had effects on the synthesis of cellular envelope components and entry into stationary phase. Due to the interconnectivity of metabolic pathways, our findings may suggest more generally that the modulation of bacterial cell shape involves the regulation of growth phase and the synthesis of cellular building blocks.

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