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Molecular Microbiology Mar 2020The peptidoglycan (PG), as the exoskeleton of most prokaryotes, maintains a defined shape and ensures cell integrity against the high internal turgor pressure. These... (Review)
Review
The peptidoglycan (PG), as the exoskeleton of most prokaryotes, maintains a defined shape and ensures cell integrity against the high internal turgor pressure. These important roles have attracted researchers to target PG metabolism in order to control bacterial infections. Most studies, however, have been performed in bacteria grown under laboratory conditions, leading to only a partial view on how the PG is synthetized in natural environments. As a case in point, PG metabolism and its regulation remain poorly understood in symbiotic and pathogenic bacteria living inside eukaryotic cells. This review focuses on the PG metabolism of intracellular bacteria, emphasizing the necessity of more in vivo studies involving the analysis of enzymes produced in the intracellular niche and the isolation of PG from bacteria residing within eukaryotic cells. The review also points to persistent infections caused by some intracellular bacterial pathogens and the extent at which the PG could contribute to establish such physiological state. Based on recent evidences, I speculate on the idea that certain structural features of the PG may facilitate attenuation of intracellular growth. Lastly, I discuss recent findings in endosymbionts supporting a cooperation between host and bacterial enzymes to assemble a mature PG.
Topics: Bacteria; Bacterial Infections; Bacterial Proteins; Cell Wall; Eukaryotic Cells; Host-Pathogen Interactions; Humans; Peptidoglycan; Symbiosis; Virulence
PubMed: 32185832
DOI: 10.1111/mmi.14452 -
Nature Reviews. Microbiology Aug 2016Electron cryotomography (ECT) enables the 3D reconstruction of intact cells in a near-native state. Images produced by ECT have led to the proposal that an ancient... (Review)
Review
Electron cryotomography (ECT) enables the 3D reconstruction of intact cells in a near-native state. Images produced by ECT have led to the proposal that an ancient sporulation-like event gave rise to the second membrane in diderm bacteria. Tomograms of sporulating monoderm and diderm bacterial cells show how sporulation can lead to the generation of diderm cells. Tomograms of Gram-negative and Gram-positive cell walls and purified sacculi suggest that they are more closely related than previously thought and support the hypothesis that they share a common origin. Mapping the distribution of cell envelope architectures onto a recent phylogenetic tree of life indicates that the diderm cell plan, and therefore the sporulation-like event that gave rise to it, must be very ancient. One explanation for this model is that during the cataclysmic transitions of the early Earth, cellular evolution may have gone through a bottleneck in which only spores survived, which implies that the last bacterial common ancestor was a spore.
Topics: Biological Evolution; Cell Membrane; Cell Wall; Gram-Negative Bacteria; Gram-Positive Bacteria; Peptidoglycan; Phylogeny; Spores, Bacterial
PubMed: 28232669
DOI: 10.1038/nrmicro.2016.85 -
Trends in Microbiology Aug 2017Bacterial cell shape is a genetically encoded and inherited feature that is optimized for efficient growth, survival, and propagation of bacteria. In addition, bacterial... (Review)
Review
Bacterial cell shape is a genetically encoded and inherited feature that is optimized for efficient growth, survival, and propagation of bacteria. In addition, bacterial cell morphology is adaptable to changes in environmental conditions. Work in recent years has demonstrated that individual features of cell shape, such as length or curvature, arise through the spatial regulation of cell wall synthesis by cytoskeletal proteins. However, the mechanisms by which these different morphogenetic factors are coordinated and how they may be globally regulated in response to cell cycle and environmental cues are only beginning to emerge. Here, we have summarized recent advances that have been made to understand morphology in the dimorphic Gram-negative bacterium Caulobacter crescentus.
Topics: Bacterial Proteins; Caulobacter crescentus; Cell Cycle; Cell Division; Cell Wall; Cytoskeletal Proteins; Cytoskeleton; Microbial Viability; Peptidoglycan; Stress, Physiological
PubMed: 28359631
DOI: 10.1016/j.tim.2017.03.006 -
MBio Aug 2022Bacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the...
Bacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the daughter cells, respectively. The cyanobacterium forms filaments of communicated cells in which the outer membrane and the peptidoglycan sacculus, which is engrossed in the intercellular regions between contiguous cells, are continuous along the filament. During the growth of , peptidoglycan incorporation was weak at the cell periphery. During cell division, midcell peptidoglycan incorporation matched the localization of the divisome, and incorporation persisted in the intercellular septa, even after the division was completed. MreB, MreC, and MreD were located throughout the cell periphery and, in contrast to other bacteria, also to the divisome all along midcell peptidoglycan growth. In mutants bearing inactivated , or genes, which showed conspicuous alterations in the filament morphology, consecutive septal bands of peptidoglycan growth were frequently not parallel to each other and were irregularly spaced along the filament, reproducing the disposition of the Z-ring. Both lateral and septal growth was impaired in strains down-expressing Z-ring components, and MreB and MreD appeared to directly interact with some divisome components. We propose that, in , association with the divisome is a way for localization of MreB, MreC, and MreD at the cell poles, where they regulate lateral, midcell, and septal peptidoglycan growth with the latter being involved in localization and maintenance of the intercellular septal-junction protein structures that mediate cell-cell communication along the filament. Peptidoglycan surrounds the bacterial cell, being essential for the determination of the bacterium-specific morphology and survival. Peptidoglycan growth has been thoroughly investigated in some model rod-shaped bacteria, and more recently some representatives with disparate morphologies became into focus, revealing that patterns of peptidoglycan growth are much more diverse than previously anticipated. forms filaments of communicated cells exhibiting features of multicellular organisms, such as the production of morphogens and coupled circadian oscillations. Here, we showed that presented a distinct pattern of peptidoglycan growth characterized by continuous incorporation of material at the polar intercellular regions, contributing to assembling and maintaining the protein complexes that expand the septal peptidoglycan mediating intercellular molecular exchange in the filament.
Topics: Anabaena; Bacterial Proteins; Cell Division; Cell Wall; Peptidoglycan
PubMed: 35876506
DOI: 10.1128/mbio.01165-22 -
MBio Jul 2019species are obligate intracellular bacteria lacking a classical peptidoglycan sacculus but relying on peptidoglycan synthesis for cytokinesis. While septal...
species are obligate intracellular bacteria lacking a classical peptidoglycan sacculus but relying on peptidoglycan synthesis for cytokinesis. While septal peptidoglycan biosynthesis seems to be regulated by MreB actin and its membrane anchor RodZ rather than FtsZ tubulin in , the mechanism of peptidoglycan remodeling is poorly understood. An amidase conserved in is able to cleave peptide stems in peptidoglycan, but it is not clear how peptidoglycan glycan strands are cleaved since no classical lytic transglycosylase is encoded in chlamydial genomes. However, a protein containing a SpoIID domain, known to possess transglycosylase activity in , is conserved in We show here that the SpoIID homologue of the -related pathogen is a septal peptidoglycan-binding protein. Moreover, we demonstrate that SpoIID acts as a lytic transglycosylase on peptidoglycan and as a muramidase on denuded glycan strands As SpoIID-like proteins are widespread in nonsporulating bacteria, SpoIID might commonly be a septal peptidoglycan remodeling protein in bacteria, including obligate intracellular pathogens, and thus might represent a promising drug target. species are obligate intracellular bacteria and important human pathogens that have a minimal division machinery lacking the proteins that are essential for bacterial division in other species, such as FtsZ. Chlamydial division requires synthesis of peptidoglycan, which forms a ring at the division septum and is rapidly turned over. However, little is known of peptidoglycan degradation, because many peptidoglycan-degrading enzymes are not encoded by chlamydial genomes. Here we show that an homologue of SpoIID, a peptidoglycan-degrading enzyme involved in sporulation of bacteria such as , is expressed in , localizes at the division septum, and degrades peptidoglycan , indicating that SpoIID is not only involved in sporulation but also likely implicated in division of some bacteria.
Topics: Amino Acid Sequence; Bacterial Proteins; Cell Division; Chlamydia; Chlamydia Infections; Chromatography, High Pressure Liquid; Gene Expression; Humans; Peptidoglycan; Protein Binding; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; Spores, Bacterial
PubMed: 31311880
DOI: 10.1128/mBio.01128-19 -
Biochemistry Jul 2018Gram-positive bacteria surround themselves with a multilayered macromolecular cell wall that is essential to cell survival and serves as a major target for antibiotics....
Gram-positive bacteria surround themselves with a multilayered macromolecular cell wall that is essential to cell survival and serves as a major target for antibiotics. The cell wall of Staphylococcus aureus is composed of two major structural components, peptidoglycan (PG) and wall teichoic acid (WTA), together creating a heterogeneous and insoluble matrix that poses a challenge to quantitative compositional analysis. Here, we present C cross polarization magic angle spinning solid-state nuclear magnetic resonance (NMR) spectra of intact cell walls, purified PG, and purified WTA. The spectra reveal the clear molecular differences in the two polymers and enable quantification of PG and WTA in isolated cell walls, an attractive alternative to estimating teichoic acid content from a phosphate analysis of completely pyrolyzed cell walls. Furthermore, we discovered that unique PG and WTA spectral signatures could be identified in whole-cell NMR spectra and used to compare PG and WTA levels among intact bacterial cell samples. The distinguishing whole-cell C NMR contributions associated with PG include the GlcNAc-MurNAc sugar carbons and glycyl α-carbons. WTA contributes carbons from the phosphoribitol backbone. Distinguishing N spectral signatures include glycyl amide nitrogens in PG and the esterified d-alanyl amine nitrogens in WTA. C NMR analysis was performed with samples at natural abundance and included 10 whole-cell sample comparisons. Changes consistent with altered PG and WTA content were detected in whole-cell spectra of bacteria harvested at different growth times and in cells treated with tunicamycin. This use of whole-cell NMR provides quantitative parameters of composition in the context of whole-cell activity.
Topics: Cell Wall; Nuclear Magnetic Resonance, Biomolecular; Peptidoglycan; Staphylococcus aureus; Teichoic Acids
PubMed: 29806458
DOI: 10.1021/acs.biochem.8b00495 -
The Journal of Biological Chemistry Jun 2023Microbial recognition is a key step in regulating the immune signaling pathways of multicellular organisms. Peptidoglycan, a component of the bacterial cell wall,...
Microbial recognition is a key step in regulating the immune signaling pathways of multicellular organisms. Peptidoglycan, a component of the bacterial cell wall, exhibits immune stimulating activity in both plants and animals. Lysin motif domain (LysMD) family proteins are ancient peptidoglycan receptors that function in bacteriophage and plants. This report focuses on defining the role of LysMD-containing proteins in animals. Here, we characterize a novel transmembrane LysMD family protein. Loss-of-function mutations at the lysMD3/4 locus in Drosophila are associated with systemic innate immune activation following challenge, so we refer to this gene as immune active (ima). We show that Ima selectively binds peptidoglycan, is enriched in cell membranes, and is necessary to regulate terminal innate immune effectors through an NF-kB-dependent pathway. Hence, Ima fulfills the key criteria of a peptidoglycan pattern recognition receptor. The human Ima ortholog, hLysMD3, exhibits similar biochemical properties. Together, these findings establish LysMD3/4 as the founding member of a novel family of animal peptidoglycan recognition proteins.
Topics: Animals; Humans; Cell Wall; Drosophila melanogaster; Drosophila Proteins; Immunity, Innate; Peptidoglycan; Membrane Proteins
PubMed: 37116706
DOI: 10.1016/j.jbc.2023.104758 -
Nature Jun 2020The primary structural component of the bacterial cell wall is peptidoglycan, which is essential for viability and the synthesis of which is the target for crucial...
The primary structural component of the bacterial cell wall is peptidoglycan, which is essential for viability and the synthesis of which is the target for crucial antibiotics. Peptidoglycan is a single macromolecule made of glycan chains crosslinked by peptide side branches that surrounds the cell, acting as a constraint to internal turgor. In Gram-positive bacteria, peptidoglycan is tens of nanometres thick, generally portrayed as a homogeneous structure that provides mechanical strength. Here we applied atomic force microscopy to interrogate the morphologically distinct Staphylococcus aureus and Bacillus subtilis species, using live cells and purified peptidoglycan. The mature surface of live cells is characterized by a landscape of large (up to 60 nm in diameter), deep (up to 23 nm) pores constituting a disordered gel of peptidoglycan. The inner peptidoglycan surface, consisting of more nascent material, is much denser, with glycan strand spacing typically less than 7 nm. The inner surface architecture is location dependent; the cylinder of B. subtilis has dense circumferential orientation, while in S. aureus and division septa for both species, peptidoglycan is dense but randomly oriented. Revealing the molecular architecture of the cell envelope frames our understanding of its mechanical properties and role as the environmental interface, providing information complementary to traditional structural biology approaches.
Topics: Bacillus subtilis; Cell Wall; Microbial Viability; Microscopy, Atomic Force; Peptidoglycan; Staphylococcus aureus
PubMed: 32523118
DOI: 10.1038/s41586-020-2236-6 -
Nature Communications Nov 2022Bacterial cell shape is generally determined through an interplay between the peptidoglycan cell wall and cytoplasmic filaments made of polymerized MreB. Indeed, some...
Bacterial cell shape is generally determined through an interplay between the peptidoglycan cell wall and cytoplasmic filaments made of polymerized MreB. Indeed, some bacteria (e.g., Mycoplasma) that lack both a cell wall and mreB genes consist of non-motile cells that are spherical or pleomorphic. However, other members of the same class Mollicutes (e.g., Spiroplasma, also lacking a cell wall) display a helical cell shape and kink-based motility, which is thought to rely on the presence of five MreB isoforms and a specific fibril protein. Here, we show that heterologous expression of Spiroplasma fibril and MreB proteins confers helical shape and kinking ability to Mycoplasma capricolum cells. Isoform MreB5 is sufficient to confer helicity and kink propagation to mycoplasma cells. Cryoelectron microscopy confirms the association of cytoplasmic MreB filaments with the plasma membrane, suggesting a direct effect on membrane curvature. However, in our experiments, the heterologous expression of MreBs and fibril did not result in efficient motility in culture broth, indicating that additional, unknown Spiroplasma components are required for swimming.
Topics: Cryoelectron Microscopy; Bacterial Proteins; Cytoskeleton; Peptidoglycan; Spiroplasma
PubMed: 36376306
DOI: 10.1038/s41467-022-34478-0 -
Advanced Science (Weinheim,... May 2022Water-responsive (WR) materials that reversibly deform in response to humidity changes show great potential for developing muscle-like actuators for miniature and...
Water-responsive (WR) materials that reversibly deform in response to humidity changes show great potential for developing muscle-like actuators for miniature and biomimetic robotics. Here, it is presented that Bacillus (B.) subtilis' peptidoglycan (PG) exhibits WR actuation energy and power densities reaching 72.6 MJ m and 9.1 MW m , respectively, orders of magnitude higher than those of frequently used actuators, such as piezoelectric actuators and dielectric elastomers. PG can deform as much as 27.2% within 110 ms, and its actuation pressure reaches ≈354.6 MPa. Surprisingly, PG exhibits an energy conversion efficiency of ≈66.8%, which can be attributed to its super-viscous nanoconfined water that efficiently translates the movement of water molecules to PG's mechanical deformation. Using PG, WR composites that can be integrated into a range of engineering structures are developed, including a robotic gripper and linear actuators, which illustrate the possibilities of using PG as building blocks for high-efficiency WR actuators.
Topics: Elastomers; Muscles; Peptidoglycan; Robotics; Water
PubMed: 35285168
DOI: 10.1002/advs.202104697