Patchiness of murein insertion into the sidewall of Escherichia coli

Pedro, Miguel A. de; Schwarz, Heinz; Koch, Arthur L.

doi:10.1099/mic.0.26125-0

Cited by 40 publications

(21 citation statements)

References 27 publications

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“…Bidirectional peptidoglycan chain synthesis also suggests that if PGTs are found in multiprotein complexes, as proposed (19), then the complexes remain stationary at biosynthetic loci rather than sliding along the membrane surface. Recent observations that new peptidoglycan is incorporated in patches throughout the bacterial sacculus (20) are consistent with such a model. It is not yet known whether catalytically active monomers can be produced if the dimerization interface is disrupted, but the structure reported here provides a basis to guide the design of experiments to address the functional role, if any, of dimerization by class A PBPs.…”

Section: Resultssupporting

confidence: 63%

Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis

Yuan

Barrett²,

Zhang³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

139

122

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Peptidoglycan is an essential polymer that forms a protective shell around bacterial cell membranes. Peptidoglycan biosynthesis is the target of many clinically used antibiotics, including the ␤-lactams, imipenems, cephalosporins, and glycopeptides. Resistance to these and other antibiotics has prompted interest in an atomic-level understanding of the enzymes that make peptidoglycan. Representative structures have been reported for most of the enzymes in the pathway. Until now, however, there have been no structures of any peptidoglycan glycosyltransferases (also known as transglycosylases), which catalyze formation of the carbohydrate chains of peptidoglycan from disaccharide subunits on the bacterial cell surface. We report here the 2.1-Å crystal structure of the peptidoglycan glycosyltransferase (PGT) domain of Aquifex aeolicus PBP1A. The structure has a different fold from all other glycosyltransferase structures reported to date, but it bears some resemblance to -lysozyme, an enzyme that degrades the carbohydrate chains of peptidoglycan. An analysis of the structure, combined with biochemical information showing that these enzymes are processive, suggests a model for glycan chain polymerization.antibiotic resistance ͉ penicillin-binding protein ͉ cell wall ͉ transglycosylase T he major component of the bacterial cell wall is a cross-linked glycopeptide polymer called peptidoglycan. This polymer surrounds the cytoplasmic membrane of bacteria and functions as an exoskeleton, maintaining cell shape and stabilizing the membrane against fluctuations in osmotic pressure. Peptidoglycan is synthesized in an intracellular phase in which UDP-Nacetylglucosamine is converted to a diphospholipid-linked disaccharide-pentapeptide known as Lipid II, and in an extracellular phase in which the disaccharide (NAG-NAM) subunits of translocated Lipid II are coupled by peptidoglycan glycosyltransferases (PGTs; also known as transglycosylases) to form linear carbohydrate chains ( Fig. 1), which are cross-linked through the attached peptide moieties by transpeptidases (1). A functioning peptidoglycan pathway is required for bacterial cell growth and division, and compounds that inhibit peptidoglycan biosynthesis have antibiotic activity (2). For example, the ␤-lactams, which have been used for decades to treat bacterial infections, irreversibly inhibit the transpeptidases. The emergence of resistance to ␤-lactams and other clinically used antibiotics has prompted intense interest in understanding peptidoglycan biosynthesis in detail. Major advances have been made in recent years with respect to the characterization of key biosynthetic enzymes (3-5). Several structures have been reported for enzymes that catalyze transpeptidation (6, 7), but no PGT structures have been described.PGTs are defined by the presence of five conserved sequence motifs ( Fig. 2A) and exist in two forms: (i) as N-terminal glycosyltransferase domains in bifunctional proteins that also contain a C-terminal transpeptidase domain [called class A penicillin-bindi...

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Section: Resultssupporting

confidence: 63%

Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis

Yuan

Barrett²,

Zhang³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

139

122

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“…To determine whether the regions enriched in MreB experienced higher levels of cell wall growth, we developed a method to quantify local cell growth. Previous single time-point electron microscopy studies suggested that new cell wall is incorporated in patches along the cylindrical cell surface (25). We reasoned that if cell surface growth is sufficiently heterogeneous, any label that binds with high affinity, is locally stationary, and has a long fluorescence lifetime could serve as a fiducial marker of cell growth in a time-lapse pulse-chase experiment.…”

Section: Resultsmentioning

confidence: 99%

Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization

Ursell

Nguyen

Monds

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

240

321

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Cells typically maintain characteristic shapes, but the mechanisms of self-organization for robust morphological maintenance remain unclear in most systems. Precise regulation of rod-like shape in Escherichia coli cells requires the MreB actin-like cytoskeleton, but the mechanism by which MreB maintains rod-like shape is unknown. Here, we use time-lapse and 3D imaging coupled with computational analysis to map the growth, geometry, and cytoskeletal organization of single bacterial cells at subcellular resolution. Our results demonstrate that feedback between cell geometry and MreB localization maintains rod-like cell shape by targeting cell wall growth to regions of negative cell wall curvature. Pulsechase labeling indicates that growth is heterogeneous and correlates spatially and temporally with MreB localization, whereas MreB inhibition results in more homogeneous growth, including growth in polar regions previously thought to be inert. Biophysical simulations establish that curvature feedback on the localization of cell wall growth is an effective mechanism for cell straightening and suggest that surface deformations caused by cell wall insertion could direct circumferential motion of MreB. Our work shows that MreB orchestrates persistent, heterogeneous growth at the subcellular scale, enabling robust, uniform growth at the cellular scale without requiring global organization.bacterial cytoskeleton | biophysical modeling | morphogenesis H ow cells maintain stable and defined morphologies is a fundamental question in all branches of life. Building cellularscale structures with the correct spatial architecture and mechanical properties requires that nanometer-scale proteins have the ability to detect and alter cell shape across multiple length scales. In walled organisms such as plants (1-5), fungi (6), and bacteria (7-10), morphogenesis is often achieved through an interplay between the cytoskeleton and cell wall synthesis. A central challenge in bacterial physiology is to understand the feedback between cell shape and the coordination of wall growth by the cytoskeleton.The cell wall plays a critical mechanical role in balancing turgor stress in virtually all bacteria and is both necessary and sufficient to define cell shape (11). The bacterial cell wall is a mesh-like network of sugar strands cross-linked by peptides (11,12). In rod-shaped Escherichia coli cells, cell wall growth occurs along the cylindrical body. Biophysical modeling has suggested that a random pattern of insertion cannot preserve cell shape (13), indicating that spatial coordination of the growth machinery is necessary for cell shape maintenance. Several lines of evidence demonstrate that the actin homolog MreB (14, 15) plays a major role in this coordination in most rod-shaped bacteria. The small molecule A22 depolymerizes MreB and causes a gradual transition from a rod-like to a spherical shape (15)(16)(17). This observation suggests that the disruption of MreB changes the patterning of new material insertion, although the nature of this...

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“…Peptidoglycan comprising the poles is, in some way, different from that in the lateral walls (52,53,55). This polar peptidoglycan is "inert" in that it is neither degraded and recycled nor diluted by addition of new material (43,52,171).…”

Section: Sequestrationmentioning

confidence: 99%

The Selective Value of Bacterial Shape

Young

2006

Microbiol Mol Biol Rev

867

777

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SUMMARY Why do bacteria have shape? Is morphology valuable or just a trivial secondary characteristic? Why should bacteria have one shape instead of another? Three broad considerations suggest that bacterial shapes are not accidental but are biologically important: cells adopt uniform morphologies from among a wide variety of possibilities, some cells modify their shape as conditions demand, and morphology can be tracked through evolutionary lineages. All of these imply that shape is a selectable feature that aids survival. The aim of this review is to spell out the physical, environmental, and biological forces that favor different bacterial morphologies and which, therefore, contribute to natural selection. Specifically, cell shape is driven by eight general considerations: nutrient access, cell division and segregation, attachment to surfaces, passive dispersal, active motility, polar differentiation, the need to escape predators, and the advantages of cellular differentiation. Bacteria respond to these forces by performing a type of calculus, integrating over a number of environmental and behavioral factors to produce a size and shape that are optimal for the circumstances in which they live. Just as we are beginning to answer how bacteria create their shapes, it seems reasonable and essential that we expand our efforts to understand why they do so.

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Patchiness of murein insertion into the sidewall of Escherichia coli

Cited by 40 publications

References 27 publications

Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis

Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis

Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization

The Selective Value of Bacterial Shape

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